skeleton

—skeletonless, adj. —skeletonlike, adj.

/skel"i tn/, n.

1. Anat., Zool. the bones of a human or an animal considered as a whole, together forming the framework of the body.

2. any of various structures forming a rigid framework in an invertebrate.

3. an emaciated person or animal.

4. a supporting framework, as of a leaf, building, or ship.

5. an outline, as of a literary work: the skeleton of the plot.

6. something reduced to its essential parts.

7. skeleton at the feast, a person or thing that casts gloom over a joyful occasion; a note or reminder of sorrow in the midst of joy.

8. skeleton in the closet or cupboard,

a. a family scandal that is concealed to avoid public disgrace.

b. any embarrassing, shameful, or damaging secret.

adj.

9. of or pertaining to a skeleton.

10. like or being a mere framework; reduced to the essential or minimal parts or numbers: a skeleton staff.

[1570-80; < NL < Gk: mummy, n. use of neut. of skeletós dried up, verbid of skéllein to dry]

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Bony framework of the body.

It includes the skull, vertebral column, collarbone, shoulder blades, rib cage, pelvic girdle and the bones of the hands, arms, feet, and legs. The skeleton supports the body and protects its internal organs. It is held together by ligaments and moved at the joints by the muscles, which are attached to it. The skeletal system includes both bones and cartilage.

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Introduction

      the supportive framework of an animal body. The skeleton of invertebrates (invertebrate), which may be either external or internal, is composed of a variety of hard nonbony substances. The more complex skeletal system of vertebrates is internal and is composed of several different types of tissues that are known collectively as connective tissues (connective tissue). This designation includes bone and the various fibrous substances that form the joints (joint), connect bone to bone and bone to muscle, enclose muscle bundles, and attach the internal organs to the supporting structure. For a more detailed discussion of the human skeleton, see skeletal system, human.

Comparative study of skeletal systems

      In addition to its supportive function, the animal skeleton may provide protection, facilitate movement, and aid in certain sensory functions. Support of the body is achieved in many protozoans (protozoan) by a simple stiff, translucent, nonliving envelope called a pellicle. In nonmoving (sessile) coelenterates, such as coral, whose colonies attain great size, it is achieved by dead structures, both internal and external, which form supporting axes. In the many groups of animals that can move, it is achieved either by external structures known as exoskeletons (exoskeleton) or by internal structures known as endoskeletons (skeleton). Many animals remain erect or in their normal resting positions by means of a hydrostatic skeleton—i.e., fluid pressure in a confined space.

      The skeleton's protective function alone may be provided by structures situated on the body surface—e.g., the lateral sclerites of centipedes (centipede) and the shell (carapace) of crabs (crab). These structures carry no muscle and form part of a protective surface armour. The scales of fish, the projecting spines of echinoderms (echinoderm) (e.g., sea urchins), the minute needlelike structures (spicules) of sponges (sponge), and the tubes of hydroids (hydroid), all raised from the body surface, are similary protective. The bones of the vertebrate skull protect the brain. In the more advanced vertebrates and invertebrates, many skeletal structures provide a rigid base for the insertion of muscles as well as providing protection.

      The skeleton facilitates movement in a variety of ways, depending on the nature of the animal. The bones of vertebrates and the exoskeletal and endoskeletal units of the cuticle of arthropods (arthropod) (e.g., insects, spiders, crabs) support opposing sets of muscles (i.e., extensors (extensor muscle) and flexors (flexor muscle)). In other animal groups the hydrostatic skeleton provides such support.

      In a limited number of animals, the hard skeleton transmits vibrations that are sensed by the hearing mechanism. In some forms—e.g., bony fishes (bony fish) and fast-swimming squids (squid)—it aids in the formation of buoyancy mechanisms that enable the animal to adjust its specific gravity for traveling at different depths in the sea.

Principal types of skeletal elements

      Certain types of skeletons usually characterize particular animal phyla, but there are a limited number of ways in which an animal can form its skeleton. Similar modes of skeleton formation have evolved independently in different groups to fulfill similar needs. The cartilaginous braincase of the octopus and the squid, which are invertebrates, has a microscopic structure similar to the cartilage of vertebrates. The calcareous (i.e., calcium-containing) internal skeleton of the echinoderms is simply constructed but is essentially not far different from the much more elaborate bones of vertebrates. Skeletal fibres of similar chemical composition occur in unrelated animal groups; for example, coiled shells of roughly similar chemical composition are present in gastropods (gastropod) (e.g., snails), brachiopods (e.g., lamp shells), and cephalopods (cephalopod) (e.g., chambered nautilus). The mechanical properties of different skeletal types vary considerably according to the needs of animals of particular size ranges or habits (e.g., aquatic, terrestrial).

      Skeletal elements are of six principal types: hard structures, semirigid structures, connective tissue, hydrostatic structures, elastic structures, and buoyancy devices.

Cuticular structures

      Hard structures may be either internal or external. They may be composed of bone (calcareous or membranous structures that are rigid), crystals, cuticle, or ossicles (i.e., minute plates, rods, or spicules).

      The scales (scale) of some fishes (fish) (e.g., sturgeon) may be heavy, forming a complete external jointed armour; calcareous deposits make them stiff. They grow at their margins, and their outer surfaces become exposed by disintegration of the covering cell layer, epithelium. Other fish scales—i.e., those of most modern bony fishes—are thin, membranous, and flexible.

Calcareous structures

      The external shells of gastropods and bivalve mollusks (mollusk) (e.g., clams, scallops) are calcareous, stiff, and almost detached from the body. The laminated, or layered, shell grows by marginal and surface additions on the inner side. Muscles (muscle) are inserted on part of the shell, and the body of the animal can be withdrawn into the protection of the shell. Chambered calcareous shells formed by cephalopods and by protozoans of the order Foraminifera become so large and so numerous that the broken remains of the shells may constitute a type of sand covering large areas of tropical beaches; the pieces may also consolidate into rock. Protozoans (protozoan) of the order Radiolaria form skeletons of silica in the form of very complicated bars. The body of the animal flows partly inside and partly outside among the bars.

       coral skeletons are also partly inside and partly outside the animal (cnidarian). Calcareous depositions below a young coral polyp (i.e., an individual member of the animal colony) are secreted by the ectoderm (generally, the outermost of three basic tissue layers), fixed to the surface to which the animal is attached, and thrown up into ridges, which form a cup into which the polyp can contract. A spreading of the base and the formation of more polyps on the base are followed by a central humping up of the soft tissue and further secretion of skeleton. An upright branch is thus formed, and, in time, large branching corals many feet high may arise from the seafloor. Most of the soft tissue is then external to an axial calcareous skeleton, but in rapidly growing corals the skeleton is perforate, and soft tissue lies both inside and outside it. Protection of the animal is provided by the skeletal cups into which each polyp can contract, but usually neither the whole colony nor a single animal has mobility.

      The starfishes, brittlestars, and crinoids (Echinodermata (echinoderm)) have many types of calcareous ossicles in the mesoderm (generally, the tissue layer between the gut and the outermost layer). These form units that articulate with each other along the arms, spines that project from the body covering and articulate with ossicles, and calcareous jaws (in sea urchins). Less well organized calcareous deposits stiffen the body wall between the arms of the starfish.

Crystals

      Crystals form the basis of many skeletons, such as the calcareous triradiate (three-armed) and quadradiate (four-armed) spicules of calcareous sponges (sponge). The cellular components of the body of the sponge usually are not rigid and have no fixed continuity; cells from the outer, inner, and middle layers of a sponge are freely mobile. Spicules, which may be of silica, often extend far from the body. They can be shed at times and replaced by new spicules. Skeletal fibres are present in many sponges.

      Calcareous spicules, large and small, form an important part of the skeleton of many coelenterates. Huge needlelike spicules, projecting beyond the soft tissue of sea pens (pennatulids), for example, both support the flanges that bear feeding polyps and hinder browsing by predators. Minute internal spicules may be jammed together to form a skeletal axis, as in the red coral. In some corals (Alcyonaria), spicules combine with fibres made of keratin (a protein also found in hair and feathers) or keratins with amorphous calcite (noncrystalline calcium carbonate) to form axial structures of great strength and size, enabling colonies to reach large bushlike proportions.

      Skeletons consisting of cuticle but remote from the body surface give support and protection to other coelenterates, the colonial sedentary hydroids, and form tubes in which pogonophores (small threadlike aquatic animals) live. Exoskeletons that are superficially similar but quite different from hydroids and pogonophores in both manner of growth and internal support occur in the graptolites (graptolite), an extinct group, and in the protochordates (protochordate), Rhabdopleura and Cephalodiscus. Some graptolites, known only from fossil skeletal remains many millions of years old, had skeletons similar to those of Rhabdopleura.

      In segmented (segmentation) and in many nonsegmented invertebrates, cuticle is secreted by the ectoderm and remains in contact with it. It is thin in annelid worms (e.g., the earthworm) and thicker in roundworms (nematodes (nematode)) and arthropods (arthropod). In many arthropods the cuticle is infolded to form endoskeletal structures of considerable complexity. Rigidity is imposed on parts of the cuticle of arthropods either by sclerotization or tanning, a process involving dehydration (as in crustaceans and insects), by calcification (as in millipedes), or by both, as in many crabs. In most arthropods the body and legs are clearly segmented. On the dorsal (upper) side of each segment is a so-called tergal sclerite of calcified or sclerotized cuticle, usually a ventral (lower) sternite and often lateral pleurites—i.e., side plates. There may be much fusion of sclerites on the same segment. Sometimes fusion occurs between dorsal sclerites of successive segments, to form rigid plates. Leg sclerotizations are usually cylindrical.

      Internally, apodemes are hollow rods or flanges derived from the cuticle; they extend inward from the exoskeleton. Apodemes have a function similar to the bones of vertebrates, for they provide sites for muscle insertion, thereby allowing the leverage that can cause movement of other parts of the skeleton independent of hydrostatic forces. The apodemal system is most fully developed in the larger and more swiftly moving arthropods. The cuticle is a dead secretion and can only increase in thickness. At intervals an arthropod molts the entire cuticle, pulling out the apodemes. The soft body rapidly swells before secreting a new, stiff cuticle. The molting process limits the upper size of cuticle-bearing animals. Arthropods can never achieve the body size of the larger vertebrates, in which the bones grow with the body, because the mechanical difficulties of molting would be too great. The mechanical properties of bone limit terrestrial mammals to about the size of a 12-ton elephant. In water, however, bone can support a heavier animal, such as a blue whale weighing 100 tons. Bone is mechanically unsuited to support an animal as bulky as, for example, a large ship.

Semirigid structures

      Flexible cuticular structures on the surface of unsegmented roundworms and arthropods are just as important in providing support as are the more rigid sclerites. Mobility between the sclerites of body and legs is maintained by regions of flexible cuticle, the arthrodial membranes. Some sclerites are stiffened by closely packed cones of sclerotization at their margins, forming structures that combine rigidity and flexibility.

      The mesoglea layer, which lies between the ectoderm and the endoderm (the innermost tissue layer) of coelenterates, is thin in small species and massive in large ones. It forms a flexible skeleton, associated with supporting muscle fibres on both the ectodermal and endodermal sides. In many branched alcyonarians, or soft corals, the mesoglea is filled with calcareous spicules, which are not tightly packed and thus permit the axis of each coral branch to bend with the swell of the sea. As a result, soft corals, which are sessile and colonial, are very strong and can resist water movements without breaking. In this respect they are unlike the calcareous corals, which break in violent currents of water. The often beautifully coloured gorgonian corals, or sea fans (sea fan), are supported by an internal horny axis of keratin. They too bend with the water movements, except when very large. In some forms the horny axis may be impregnated with lime. The horny axes are often orientated in complex branches set in one plane, so that the coral forms a feeding net across a prevailing current. Certain chordates (chordate) also possess a flexible endoskeleton; the rodlike notochord occurs in adult lampreys (lamprey) and in most young fishes. Running just within the dorsal midline, it provides a mechanical basis for their swimming movements. In the higher vertebrates the notochord is surrounded by cartilage and finally replaced by bone. In many protochordates, however, the notochord remains unchanged. cartilage too forms flexible parts of the endoskeletal system of vertebrates, such as between articulating bones and forming sections of ribs.

connective tissue

      Below the ectoderm of many animals, connective tissue forms sheets of varying complexity, existing as fine membranes or as complex superficial layers of fibres. Muscles inserted on the fibres form subepithelial complexes in many invertebrates; and vertebrate muscles are often inserted on firm sheets of connective tissue (fascia) deep in the body that are also formed by these fibres. Particular concentrations of collagen fibres, oriented in different directions, occur superficially in the soft-bodied Peripatus (a caterpillar-like terrestrial invertebrate). In coelenterates they also occur deep in the body. In many arthropods (arthropod), collagen fibres form substantial endosternites (i.e., ridges on the inner surface of the exoskeleton in the region of the thorax) that are isolated from other skeletal structures. These fibres are not shed during molting, and the endosternites grow with the body. The fibres do not stretch, but their arrangement provides firm support for muscles and sometimes permits great changes in body shape.

The hydrostatic skeleton

      The hydrostatic skeleton is made possible by closed fluid-filled internal spaces of the body. It is of great importance in a wide variety of animal groups because it permits the antagonistic action of muscles used in locomotion and other movements. The fluid spaces are part of the gastrovascular cavity in the Coelenterata, part of the coelomic cavity (between the gut and the body wall) in the worms, and hemocoelic (i.e., in a type of body cavity consisting of a complex of spaces between tissues and organs) or vascular in mollusks and arthropods. As the exoskeleton becomes more rigid and the apodemal endoskeleton more fully developed in arthropods, the importance of the hemocoele in promoting antagonistic muscle action decreases. In larger and more heavily sclerotized species, the hydrostatic skeleton is no longer of locomotory significance; the muscles work directly against the articulated skeleton, as in vertebrates.

Elastic structures

      In the larger medusae (medusa), or jellyfishes (jellyfish) (Coelenterata), the musculature is mainly circular. By contracting its bell-shaped body, the jellyfish narrows, ejecting water from under the bell; this pushes the animal in the opposite direction from that of the water. There are no antagonistic muscles to counteract the contracted circular muscles. A passive, slow return of the bell to its expanded shape is effected largely by the elasticity of the mesoglea layer, which crumples during the propulsive contraction. After the circular muscles relax, the distorted mesoglea fibres pull them out to expand the bell. In many of the larger mammals, elastic fibres are used more extensively. The elephant and the whale, for example, possess an abundance of elastic tissue in their musculature.

      Elasticity of surface cuticle assists recovery movements in roundworms and arthropods, but the stresses and strains that cuticle can withstand are limited. Special sensory devices (chordotonal organs) convey the extent of stress in the cuticle to the animal's nervous system, thus preventing the generation of stresses great enough to damage the structure. There are also elastic units in the base of the wings of some insects (insect). These rather solid elastic structures alternately store and release energy. They have probably been important in the evolution of the extremely rapid wingbeat of some insects.

Buoyancy devices

      Buoyancy devices are complex structures that involve both hard and soft parts of the animal. In vertebrates they may be closely associated with or form part of the auditory apparatus. A chain of auditory ossicles in mammals transmits vibrations from the tympanic membrane to the internal ear (ear, human); simpler devices occur in the cold-blooded land vertebrates. In the roach fish, which has sensitive hearing, a chain of four Weberian ossicles (Weberian apparatus) connects the anterior, or forward, end of the swim bladder to the auditory organs of the head. Sound vibrations cause changes in volume in the anterior part of the bladder and are transmitted to the nervous system through the ossicles. The swim bladder of other fishes appears to be a buoyancy organ and not skeletal; however, cephalopods (cephalopod) capable of swimming rapidly in both deep and shallow water possess air-filled buoyancy organs. The calcareous coiled shell of the bottom-dwelling nautilus is heavy and chambered; the animal lives in the large chamber. The shell behind is coiled and composed of air-filled chambers that maintain the animal in an erect position. When the entire coiled, lightly constructed shell of Spirula sinks into the body, the animal has internal air spaces that can control its buoyancy and also its direction of swimming. In cuttlefish and squids (squid), a shell that was originally chambered has become transformed into a laminated cuttlebone. Secretion and absorption of gases to and from the cuttlebone by the bloodstream provide a hydrostatic buoyancy mechanism that enables the squids to swim with little effort at various depths. This device has probably made it possible for some species to grow to a length of 18 metres (59 feet). Some siphonophores (Coelenterata) have a chambered gas-filled float, its walls stiffened with a chitinlike structure in Velella.

Varieties of invertebrate skeletons

Skeletomusculature of a mobile coelenterate

      A sea anemone provides an example of the way in which a hydrostatic skeleton can act as the means by which simple sheets of longitudinal and circular muscle fibres can antagonize each other to produce contrasting movements. The fluid-filled space is the large digestive, or internal, cavity of the body. If the mouth is slightly open when both longitudinal and circular muscles of the trunk contract, fluid flows out of the internal space, and the body shrinks. If the mouth is closed, the internal fluid-filled space cannot be compressed; thus, the body volume remains constant, and contraction of the longitudinal muscles of the trunk both shortens and widens the body. Contraction of the circular muscles pulls out relaxed longitudinal muscles, and the body lengthens. Appropriate coordination of muscular action working against the hydrostatic skeleton can produce locomotion movements—such as burrowing in sand or stepping along a hard surface—by billowing out one side of the base of the animal while the other side of the base contracts, forcing fluid into the relaxed, dilated portion. The forward dilated part sticks to the surface, and its muscles contract, pulling the animal forward.

      The circular muscles lie outside a substantial layer of skeletal mesoglea fibrils; longitudinal muscles are internal to the layer. The muscle fibres are attached at either end to the mesoglea fibres, which, like vertebrate bones, cannot stretch. Unlike bones, however, the mesoglea sheet is able to change its shape, because its components (fibrils) are set in layers at an angle to each other and to the long axis of the body. Alteration in length and width of the body is accompanied by changes in the angle between two sheets of mesoglea fibrils; thus, support for the muscles can vary greatly in position. The range in change of shape of the sea anemone is implemented by simple muscles and connective-tissue mesoglea fibrils. The movements are characteristically slow, often occurring so slowly as to be invisible to the naked eye. Faster movements would engender greater increases in internal pressures, thus placing a needless burden on the musculature. All coelenterates utilize this slow hydrostatic-muscular system, but, as described for the jellyfish, some faster movements are also possible.

Skeletomusculature of an earthworm

      The hydrostatic skeleton of many other animals is provided by the body cavity, or coelom, which is situated outside the alimentary canal and inside the body wall. In an earthworm the body cavity of each segment of the trunk is separated from that of the next by a partition, so that the segmented body possesses a series of more or less isolated coelomic, fluid-filled spaces of fixed volume. The body wall contains circular and longitudinal muscles and some minor muscles. As in the sea anemone, skeletal connective-tissue fibres form the muscle insertions. As a worm crawls or burrows, a group of segments shorten and widen, their total volume remaining the same; contact with the ground is maintained by projection of bristlelike structures from the cuticle (setae). Groups of short, wide segments are formed at intervals along the body; the segments between these groups are longer, narrower, and not in contact with the ground. As the worm crawls, the thickened zones appear to travel backward along the body, because the segments just behind each zone thicken, widen, and cling to the ground, while the segments at the front end of each wide zone free themselves from the ground and become longer and narrower. Thus, the head end of the body intermittently progresses forward over the ground or enters a crevice as the longitudinally extending segments are continuously being lengthened outward from the front end of each thickened zone. It is therefore only the long, narrow segments that are moving forward. This mechanism of crawling by the alternate and antagonistic action of the longitudinal and circular muscles is made possible by the hydrostatic action of the incompressible coelomic spaces. The movements of most other annelid worms are also controlled by a hydrostatic skeleton.

Skeletomusculature of arthropods

      In arthropods (arthropod) the skeleton is formed in part by the cuticle covering the body surface, by internal connective-tissue fibres, and by a hydrostatic skeleton formed by the hemocoele, or enlarged blood-filled spaces. The cuticle may be flexible or stiff, but it does not stretch. In the Onychophora (velvet worm) (e.g., Peripatus) the cuticle is thin and much-folded, thus allowing great changes in the body shape. The muscular body wall, as in annelids, works against the hydrostatic skeleton in the hemocoele. Each leg moves in a manner similar to the body movement of a sea anemone or a Hydra. But a unique lateral isolating mechanism allows suitable hydrostatic pressures to be available for each leg. Muscles of a particular leg thus can be used independently, no matter what the other legs may be doing or what influence the body movements may be having on the general hemocoele.

      In most adult arthropods the cuticle is less flexible than in the Onychophora: localized stiff sclerites are separated by flexible joints between them, and, as a result, the hydrostatic action of the hemocoele is of less importance. cuticle, secreted by the ectodermal cells, may be stiffened by deposition of lime or by tanning (sclerotization). Muscle fibres or their connective-tissue supports are connected to the cuticle by tonofibrils within the cytoplasm of ectodermal cells.

      The joints between the stiffened sclerites consist of undifferentiated flexible cuticle. Between the distal (i.e., away from the central body axis) leg segments of many arthropods (arthropod), the flexible cuticle at the joint is relatively large ventrally (i.e., on the lower side) and very short dorsally (i.e., on the upper side), thus forming a dorsal hinge. Flexor muscles (flexor muscle) (for drawing the limb toward the body) span the joint and cause flexure of the distal part of the leg. There are no extensor muscles (extensor muscle), however, and straightening of the leg when it is off the ground is effected by hydrostatic pressure of the general hemocoele and by proximal depressor muscles that open the joint indirectly. Between the proximal leg segments (i.e., those closer to the point of insertion of the limb into the body), pivot joints are usually present. They are composed of a pair of imbricating facets near the edges of the overlapping cylinders that cover the leg segments, with one pair on the anterior face of the leg and another on the posterior face. A pair of antagonistic muscles span the leg joint and move the distal segment up or down, without reference to hydrostatic pressure.

      The more-advanced arthropods—those with the most elaborate sclerites and joints—are no longer dependent upon hydrostatic forces for skeletomuscular action. Evolution away from the hydrostatic skeleton has made possible faster and stronger movements of one cuticular unit upon another. The type of skeletomusculature appropriate for producing fast movements, such as rapid running, jumping, or flying, is quite different from those producing strong movements, such as those used by burrowing arthropods.

      The flexible edges of the sclerites of burrowing centipedes (centipede) (Geophilomorpha) enable them to change their shape in an earthwormlike manner while preserving a complete armour of surface sclerites at all times. The marginal zones of the sclerites bear cones of sclerotization that are set in the flexible cuticle, thus permitting flexure in any direction without impairing strength. The surface of the arthropodan cuticle is rendered waterproof, or hydrofuge, by a variety of structures, such as waxy layers, scales, and hairs. These features enable the animals not only to resist desiccation on land but to exist in damp places without uptake of water—a process that could cause swelling of the body and lead to death. The cuticular endoskeleton is formed by an infolding of surface cuticle. Sometimes a large surface sclerite called a carapace covers both the head and the thorax, as in crabs and lobsters.

      Connective-tissue fibres form substantial endoskeletal units in arthropods. The fibres are not united to the cuticle and are not shed during molting; rather, they grow with the body. A massive and compact endosternite (internal sternite), formed by connective-tissue fibres, frequently lies below the gut and above the nerve cord. In Limulus, the horseshoe crab, muscles from the anterior margin of the coxa (the leg segment nearest the body) are inserted on the endosternite, as are other muscles from the posterior margin.

      The jointed cuticular skeleton of arthropods enables them to attain considerable size, up to a few metres in length, and to move rapidly. These animals have solved most of the problems presented by life on dry land in a manner unequaled by any other group of invertebrates. They have also evolved efficient flight by means of wings derived from the cuticle. The arthropods can never achieve the body size of the larger vertebrates, although mechanically they perform as well as smaller vertebrates. As mentioned above, the major limiting factor to size increase is the need to molt the exoskeleton.

Skeleton of echinoderms (echinoderm)

      Among the invertebrates, only the echinoderms (echinoderm) possess an extensive mesodermal skeleton that is stiffened by calcification—as in vertebrates—and also grows with the body. The five-rayed symmetry of echinoderms may be likened to the vertebral axis of vertebrates. It is similarly supported; a series of ambulacral ossicles in each ray roughly corresponds with the vertebrae of vertebrates. The ossicles articulate with each other in mobile echinoderms such as starfishes (sea star) and form the basis of the rapid movements of the arms of crinoids, brittlestars, and similar forms. The ambulacral ossicles and, in many cases, the surface spines provide protection for superficial nerve cords, which extend along the arms and around the mouth. The ossicles also protect the tubes of the water-vascular system, a hydraulic apparatus peculiar to echinoderms. In sea urchins (sea urchin) a spherical, rigid body is formed by the five arms coming together dorsally around the anus; the ambulacral ossicles are immobile, and the body wall between the ambulacra is made rigid by a layer of calcareous plates below the ectoderm, which completes the continuous spherical skeleton. Locomotion is carried out by extensible tube feet, soft structures that are pendant from the water-vascular system. Mobile spines also serve for locomotion in many classes, the base of the spine articulating with a part of some stable ossicle. The fine internal structure of echinoderm sclerites bears no resemblance to that of bone.

Sidnie M. Manton

The vertebrate skeleton

General characteristics

      In vertebrates (vertebrate) the adult skeleton is usually formed of bone or cartilage—living substances that grow with the animal, in contrast to the many types of invertebrate skeleton that do not grow or are dead secretions, deposits, or crystals. The internal position of bones and their central position in limbs provide firm support for small and large animals. Muscles can be inserted on all surfaces of the skeleton, in contrast to the limitations of the cuticular skeleton of arthropods, in which muscles occur on only one side. Antagonistic muscles are easily placed upon vertebrate bones to allow contrasting movements at the joints between them.

      The component parts of the skeletons of vertebrates, although remarkably uniform in basic plan, are subject to wide superficial differences, which are associated with each class and with adaptations for particular habits or environments. The axial skeleton consists of the skull and the vertebral column. The appendicular skeleton supports the fins in fish and the legs in tetrapods (four-legged animals) and is associated with limb girdles, which become progressively more closely linked with the vertebral column in the higher vertebrates. Superficially there may be an exoskeleton of scales; some scales on the head may be incorporated into the skull.

      Swimming (aquatic locomotion) of a typical fish occurs by undulations passing along a greater or lesser part of the body. The mechanism for caudal (tail) propulsion involves the vertebral column, the axial musculature, and the lateral surfaces of the body and caudal fin. The vertebral column of the fish can be regarded as a series of rigid units hinged to each other by surfaces that allow the body to bend only sideways. On each side of the vertebral chain lie the great axial muscles of the body; the fibres of this complex group of muscles are more or less parallel to the long axes of the vertebrae. One pair of vertebrae and its associated musculature form the fundamental unit of propulsion. The muscles on the two sides of each vertebral articulation shorten alternately, the surface of the body becoming concave, or bent inward, on the side on which the muscles are shortened and convex, or bent outward, on the side on which they are stretched. The whole tail of the fish is essentially a chain of such units in which the phase of muscular contraction at any one link is slightly ahead of that of the next posterior unit and slightly behind that of the next anterior unit. Each wave of contraction passes tailward along the body, which is thus propelled forward. The greatest thrust against the water is exerted by the tail end. Ribs of various kinds lie between and support the segmental muscles. The fins and their skeletal supports are used as balancing and steering organs. The paired fins are set horizontally in cartilaginous fish, which do not have a swim bladder, and vertically in most bony fishes, in which rapid vibrations or small angular movements provide exact steering. In the air-breathing lungfish, fins are used for stepping on the bottom in a manner that superficially resembles stepping by the legs of a salamander. Indeed, the land vertebrates evolved from extinct fishes that used their fins for stepping; the pentadactyl (i.e., with five digits) skeleton and the form of the forelegs and hind legs of land vertebrates similarly evolved from the fins of such fishes.

      An unjointed elastic notochord is present in the protochordate amphioxus, in the tail of larval ascidians (tunicates (tunicate)), and in the adult cyclostomes (cyclostome) (lamprey and hagfish), but there are no vertebrae. Segmental series of muscles are present as in fish, and the resultant swimming movements of these muscles, working with the elastic notochord, are similar to those in fish.

      The lateral body undulations caused by the trunk musculature, as seen in fish, are the main propulsive agents in amphibians (amphibian) such as the newt. The feet raise the body from the ground but otherwise serve only to anchor the body, while the vertebral musculature allows forward progression by straightening the flank. The same propulsive mechanism serves for locomotion in water and on land. In the reptiles, birds, and mammals, a transition of the locomotory force from the body to the limbs occurs. When the vertebral muscles contract isometrically (i.e., against such great pressure that the muscle is unable to shorten) so as to prevent body undulations, the energy for propulsion comes from the limbs. Hands and feet are directed forward, as is the knee; and the elbow is directed backward. The limbs are no longer outstretched laterally but move ventrally below the body. The bones at the heel and elbow are extended to form levers that give origin to powerful extensor muscles of the foot and hand, thus contributing to a locomotory thrust against the ground. The elimination of lateral undulations of the vertebral column as the main propulsive agent is accompanied by the development of dorsoventral flexibility of the chain of vertebrae; the distance between successive footfalls is less if the vertebral column remains rigid.

      Swimming in whales (whale) is accomplished by means of dorsoventral tail beats, in contrast to swimming in fish, which beat the tail laterally. The swimming musculature of whales evolved from the nonswimming musculature of terrestrial ancestors. Long antagonistic muscles extend from the whale's skull to the tail and implement the dorsoventral motion, in contrast to propulsion by means of segmental muscles in fish.

      The structure of the vertebrae provides a basis for many movements, including those mentioned above. Mobility sometimes is extreme, as in the necks of certain birds, in which the imbricating, or overlapping, centra (i.e., the main ventral portion of a vertebra that articulates with that of the adjacent vertebrae) can flex in any direction yet remain firmly interlocked, because the adjacent articular surface of the bony centra is saddle-shaped. The extensive mobility of snakes (snake) is mediated by their vertebral structure and their well-developed ribs; in this case, some mobility is lost, but greater stability is achieved by fusion of two or more vertebrae.

      The limbs of tetrapods and their limb girdles have become much-modified in association with particular habits, such as rapid running (terrestrial locomotion), jumping, swimming, and burrowing. The limb bones remain relatively unspecialized in slow-moving animals and in those with climbing ability. Accomplished runners differ from humans and monkeys in that the proximal sector of the leg— humerus in the forelimb, femur in the hind limb; i.e., the portion closer to the limb's insertion in the body proper—is short. This sector carries many locomotory muscles but does not project far—if at all—from the trunk. Beyond the short, strong femur and humerus, the limb bones of running animals are elongated, slender, and strong. The distal part of the leg (i.e., that portion farther from the trunk) must be narrow and light if it is to move rapidly through a wide angle. The wrist and knee are far from the ground, and in horses (horse) and other ungulates (ungulate) (i.e., hoofed animals) the animal stands on its toenails and fingernails (hooves); the whole hand and foot are raised from the ground, thus contributing to leg length.

embryology of vertebrate skeletons

      When the early embryo consists of only two tissue layers, ectoderm and endoderm, a longitudinal thickening appears as the result of multiplication of the ectodermal cells. This thickening, the primitive streak, gives rise to the notochord and to the third basic layer, the mesoderm. The longitudinal axis of the embryo is first laid down by the formation of a cylindrical mass of cells, the notochord, proliferated from the primitive (Hensen) node at the anterior end of the streak. The notochord lies ventral to the developing central nervous system and forms the first supporting structure for the developing embryo.

      In fishes such as the shark, cartilaginous vertebrae form around the notochord and to some extent compress it. It persists, nevertheless, as a continuous structure through the length of the vertebral column. In the higher vertebrates, including humans, the notochord is a temporary structure, persisting only as a minute canal in the bodies of the vertebrae and in the central part of the nucleus pulposus of the intervertebral disks.

      As the notochord is being laid down, cells proliferate from each side of the primitive streak, forming the mesoderm, which spreads out laterally and, as a result of migration and multiplication of cells, soon comes to occupy most of the space between the ectoderm and the endoderm on each side of the notochord. The mesodermal sheets soon become differentiated into (1) a mass lying on each side of the notochord (paraxial mass) that undergoes segmentation into hollow blocks, the mesodermal somites, (2) a lateral plate that becomes separated into an outer layer, the somatopleuric mesoderm, against the future body wall and an inner layer, the splanchnopleuric mesoderm, against the endoderm of the future gut, and (3) an intermediate mass, the nephrogenic cord, which gives rise mainly to the genitourinary system.

      The segmentation of the paraxial mesoderm is a fundamental feature of the development of the vertebrates. The axial skeleton and associated structures develop from part of the mesodermal somite; the appendicular skeleton arises from the somatopleuric mesoderm of the lateral plate. Each somite differentiates into (1) a lateral and superficial plaque, the dermatome, which gives rise to the integumentary tissue (integument), (2) a deeper lateral mass, the myotome, which gives rise to the muscles (muscle), and (3) a medial ventral mass, the sclerotome. The sclerotomic cells from each pair of somites migrate until they enclose the notochord, separating it from the neural tube dorsally and from the aorta (the principal blood vessel) ventrally. The sclerotomic tissue retains its original segmentation and condenses to form the forerunner, or blastema, of the centrum of the future vertebra. From each posterolateral half of the condensation, extensions pass backward and eventually meet posteriorly around the neural tube to form the blastema of the neural (dorsal) arch of the vertebra. In the interspaces between adjacent myotomes of each side, an extension from each sclerotomic mass passes laterally and forward to form the costal, or rib, element. It is only in the thoracic (midbody) region that the costal elements develop into ribs. In the other regions the costal elements remain rudimentary (undeveloped).

      The mesenchymal blastema of the future vertebra becomes chondrified; i.e., the mesenchymal cells are converted into cartilage cells. In this cartilaginous vertebra, ossification (bone-forming) centres appear, and the cartilage is gradually replaced by bone. The mesenchyme of the embryonic ribs also undergoes chondrification and later ossification. In the thoracic region, in which costal elements are best developed, a cartilaginous sternal bar forms, connecting the anterior, or growing, ends.

      The appendicular skeleton begins to develop in the primitive limb bud in the core of mesenchyme that is derived directly from the unsegmented somatopleuric mesoderm. This mesenchyme condenses to form the blastemal masses of the future limb bones. Soon the mesenchyme becomes transformed into the cartilaginous precursors of the individual bones (except in the clavicle). The cartilaginous models determine the general shape and relative size of the bones. There is convincing evidence that the shape of the bones of higher vertebrates is determined by factors inherent in the tissues and that, once development has begun, extrinsic influences provide the proper conditions for maintaining the normal structure.

      The first mesenchymal condensations of the appendicular skeleton are in the region of the future girdles; those for the shoulder girdle appear a little earlier than those for the pelvic girdle. The mesenchymal condensations for the other bones of the limbs appear in order of their proximity to the trunk.

Evolution of the vertebrate skeleton

vertebral column and thoracic skeleton

      The notochord, which constitutes the earliest structure that stiffens the embryo, appeared in animals before the true vertebral column evolved. A vertebra includes a centrum and a neural arch surrounding the spinal cord.

Lower chordates (chordate) and fishes

      Possession of the notochord is what distinguishes members of the most-advanced phylum, Chordata. In the sea squirts (sea squirt) (Urochordata), the notochord is present in the tail region of the larva but disappears after the animal transforms into the adult. In amphioxus (Cephalochordata), the notochord is permanent and extends the whole length of the body. In the cyclostome fishes (Agnatha), the most primitive group within the subphylum Vertebrata, the notochord and its sheath persist throughout life; rudimentary cartilaginous neural arches are found in the adult lamprey. Among the sharks (shark) (Selachii), modern representatives possess a vertebral column composed of cartilaginous, partly calcified centra that have their origin within the sheath of the notochord, thus causing its partial absorption. Among the bony fishes (bony fish) (Osteichthyes), the sturgeon possesses a persistent notochord with a fibrous sheath, upon which appear paired cartilaginous arches—dorsally, the neural arches; and ventrally, the hemal arches. The vertebrae of the more advanced bony fishes, such as the salmon and the cod, are completely ossified; each centrum develops in the sclerotomic mesoderm outside the notochordal sheath, a phenomenon known as perichordal development.

Amphibians (amphibian) and higher vertebrates

      In amphibians (amphibian) a vertebra is formed from the sclerotomic tissues of two somites, the tissue from the posterior part of one somite joining that from the anterior part of the somite behind it. In modern reptiles (reptile) the vertebrae are completely ossified. The neural arch has a spinous process and pre- and post-zygapophyses (additional articulating surfaces); at the junction of the arch and centrum is a facet for articulation of the head of a rib. Groups of vertebrae can be distinguished; e.g., the cervical vertebrae are recognizable because the neck is differentiated from the body.

      The fibrocartilaginous intervertebral disks uniting the centra of crocodiles (crocodile) have been identified as representing so-called intercentra. Ribs are present in the cervical, thoracic, and lumbar regions of the column.

      The sternum may be calcified in the reptiles (reptile) but is seldom ossified. In the lizards (lizard) it is a cartilaginous plate articulated with the coracoid processes of the pectoral girdle and with the anterior thoracic ribs. The sternum is absent in the turtles (turtle) and in the snakes (snake); in the crocodiles it is a wide plate joined by the coracoid processes and by two pairs of ribs.

      The skeletons of modern birds (bird) show reptilian features with some specialized adaptations to their bipedal locomotion (i.e., by means of one pair of legs) and their power of flight. The neck is very flexible. With its variation in length, the number of cervical vertebrae ranges from 25 in the swan to 9 in certain small birds. The tendency for the vertebrae to fuse in certain regions is characteristic of birds. The sternum, a very large bone, is positioned like a shield in front of the chest. In flying birds a median keel, the carina, projects ventrally, providing additional surface for the attachment of the pectoral muscles that move the wings. The flightless birds, such as the ostrich, have a keelless, raftlike sternum.

      In mammals (mammal) the vertebral centra articulate by means of intervertebral disks of fibrocartilage. Bony disks (epiphyses) formed on the generally flat ends of the centra are characteristic of mammals. Regional differentiation in the mammalian backbone is marked. The number of vertebrae in each group, excepting the caudal vertebrae, is moderately consistent, though there are some exceptions to the group averages. Whereas 7 cervical vertebrae are the rule, there are 9 or 10 of them in the three-toed sloth and only 6 in the two-toed sloth and the manatee. The thoracic vertebrae commonly number 13 or 14, although the number varies from 9 in some whales to 24 in the two-toed sloth. The average number of lumbar vertebrae is approximately 6, but there are 2 in the duck-billed platypus and 21 in the dolphin. Rib elements are fused to the transverse processes of the cervical vertebrae, and in the lumbar vertebrae they form the so-called transverse processes.

      There is an increase in the number of vertebrae that compose the sacrum. In the early developmental stages of the human fetus, the beginnings of the hip bones lie opposite those segments of the spinal column that form the lower lumbar and upper sacral vertebrae. As development proceeds, the sacroiliac joints become established between the hip bones and the upper sacral vertebrae. The sacrum, derived from the 25th to the 29th vertebrae, inclusive, becomes a single bone by their fusion. The whales and sea cows (sea cow) lack a sacrum, although vestiges of a pelvis occur. In some anteaters (anteater) the posterior sacral vertebrae are fused with the ischium (a bone on each side of the pelvic girdle) through ossification of a connecting ligament. The sacrum of some armadillos (armadillo) consists of 13 vertebrae, caudal vertebrae having become fused with it. The cervical vertebrae of some whales are fused together, because the whale is spindle-shaped for swimming and has no need for a mobile neck such as occurs in most mammals. The centrum of the atlas (first cervical vertebra) of most mammals fuses with that of the axis (second cervical vertebra) and projects from it, but in the duckbilled platypus, as in the reptiles, it is a separate bone.

      The spinous processes of the thoracic vertebrae, excepting the last, point caudally (i.e., toward the tail), while those of the lumbar vertebrae generally point cranially (i.e., toward the head) at the transitional zone between these groups. Spines of one or two thoracic vertebrae are upright; these are known as anticlinal spines. Lying ventral to the intervertebral disks in some mammals (e.g., whale, pangolin) are paired ossicles, the intercentra, which are homologous (of similar origin) with the anterior arch of the atlas. The tail vertebrae vary in number from none in the bat to 49 in the pangolin.

      The ribs in mammals correspond in number of pairs to the number of thoracic vertebrae. The ventral ends of the ribs join the costal cartilages, the relations of which follow, with minor variations, the pattern for the human skeleton. Sternal ribs, connecting the more anterior vertebral ribs with the sternum, may be cartilaginous, calcified, or ossified. The mammalian sternum is composed of several pieces: the presternum anteriorly, followed by the mesosternum, made up of a number of segments, and a terminal xiphisternum.

Appendicular skeleton

General features

      Paired appendages are not found in ancestral vertebrates and are not present in the modern cyclostomes (cyclostome) (e.g., lampreys, hagfishes). Appendages first appeared during the early evolution of the fishes (fish). Usually two pairs of appendages are present, fins in fish and limbs in land vertebrates. Each appendage includes not only the skeletal elements within the free portion of the limb but also the basal supporting structure, the limb girdle. This portion of the appendage lies partly or wholly within the trunk and forms a stable base for the fin or limb. Each girdle consists of ventral and dorsal masses. In lower fishes these are composed of cartilage; in bony fishes and in land vertebrates they become partly or completely ossified.

      The anterior appendages, the pectoral fins or forelimbs, articulate with the pectoral girdle. The pectoral girdle is situated just behind the gill region in fish and in a comparable position at the junction of the neck and thorax in land vertebrates.

      The posterior appendages, called pelvic fins or hind limbs, articulate with the pelvic girdle, which is situated in the trunk region usually just in front of the anus or cloaca (the ventral posterior body opening in many lower vertebrates). It is by way of the girdles that the weight of the body of land vertebrates is transmitted to the limbs. Because the hind limb is usually of greater importance in weight bearing, especially in bipedal vertebrates, it articulates with the vertebral column by means of the costal elements of the sacral vertebrae. The vertebrae to which the pelvic girdle are attached usually fuse together to form the sacrum. In fishes, however, a sacrum as such does not develop, owing to the fact that the posterior appendages usually do not support the body weight but are used only in locomotion.

      The origin of paired fins has been much debated, and many theories have been put forward in explanation. According to the widely accepted fin-fold theory, the paired limbs are derived from the local persistence of parts of a continuous fold that in ancestral (evolution) vertebrates passed along each side of the trunk and fused behind the anus into a single fin. The primitive paired fins were attached to the body by a broad base and carried no weight. Their main function, it would appear, was to act as horizontal stabilizing keels, which tended to prevent rolling movements and possibly also front-to-back pitching movements.

      Most authorities agree that the limbs of land vertebrates evolved from the paired fins of fishes. Limbs and fins are thought to have their ancestral counterparts in the fins of certain lobe-finned fishes (Crossopterygii, a nearly extinct group of which the coelacanth is a living example). The skeleton of the primitive fin consists of a series of endoskeletal rods, each of which undergoes subdivision into a series of three or four pieces. The basal pieces tend to fuse into larger pieces. The most anterior of the basal pieces fuses across the midline with its fellow of the opposite side to form a primitive girdle that is in the form of a cartilaginous bar. The more distal basal pieces remain separate, forming the dermal (i.e., on or near the body surface) fin rays.

Pectoral girdle

      In a cartilaginous fish, such as the dogfish, the pectoral girdle consists of a U-shaped endoskeletal, cartilaginous, inverted arch with its ends extending dorsally.

      In all other major groups of vertebrates, the pectoral girdle is a composite structure. It consists of endoskeletal structures to which secondary dermal components are added as the result of ossification of dermal elements. The components become ossified to form dermal bones. In primitive bony fishes—such as the lungfishes, sturgeon, and coelacanths—the main element added is a vertically placed structure, the cleithrum, which supports the scapula. The cleithrum may be joined by a supracleithrum, which in turn is surmounted by a posttemporal element (i.e., at the rear of the skull). The most ventral of the added dermal bones are the clavicles (clavicle), which unite below the gill chambers with each other or with the sternum. In the holostean fishes (e.g., gar) the clavicle is lost, leaving only the cleithrum.

      In tailed amphibians, such as newts (newt) and salamanders (salamander), the dermal elements of the pectoral girdle have been completely lost, and only the endoskeletal parts remain, mainly in the form of cartilaginous bars. This retrogression is probably the result of their adaptation chiefly to an aquatic mode of life, in which less support is required by the girdles. The ventral part of the girdle forms the coracoid process, and the dorsal part forms the scapula; the latter is the only part that ossifies. Only a rudimentary sternum develops.

      In most reptiles (reptile) the primary girdle for the forelimb consists of a scapula and a single coracoid process. The pectoral girdle of the lizard consists of bones formed in cartilage—the scapula and the large coracoid process, forming the glenoid cavity (i.e., the cup-shaped structure in which the humerus articulates)—and the dermal bones—the clavicle and interclavicle. The latter is a single T-shaped bone, with the stem in the midline; it is in contact with the sternum. The curved clavicles articulate with each other at their medial ends (i.e., toward the body midline). The cartilaginous suprascapula is present.

      In birds (bird) the pectoral girdle is essentially similar to that in reptiles. The precoracoid process forms a stout bar that reaches to the sternum. The wishbone, or furcula, which forms from the dermal part of the girdle, consists of two clavicles united in the midline by the interclavicle. Carinate birds (those with a keeled sternum) possess a sabre-shaped scapula and a stout coracoid process, joined by ligaments at the point at which is found the glenoid cavity for articulation with the humerus. The coracoid process is joined to the sternum; at its dorsal end is the acrocoracoid process. The furcula stands in front of the coracoid processes. The furcula's ends are connected by ligaments with the acrocoracoid process and with the rudimentary acromion process of the scapula. The girdle of the flightless ratite birds (those with a flat sternum) is little developed. The girdle is represented by an ankylosed, or fused, scapula and coracoid process.

      Among mammals (mammal), the monotremes (monotreme) have two coracoid processes, which articulate medially with the presternum and laterally with the scapula. The coracoids enter into the formation of the glenoid cavity. Also present are an interclavicle (episternum) and an investing clavicle, resembling the bones in reptiles. The clavicle articulates with the acromion process of the scapula. In the opossum the scapula has a spine ending in the acromion, with which the clavicle articulates. A much-reduced coracoid fuses with the scapula and does not meet the sternum. The scapula of placental mammals has a spine ending, generally, in an acromion; the body of the bone is triangular. In mammals that use the forelimb for support in standing, the vertebral margin is the shortest, and the long axis of the scapula runs from it to the glenoid cavity; but in those whose forelimb is used for prehension, or grasping, such as in the primates, or for flight, such as in the bats (bat), the vertebral margin is elongated, and the distance from it to the glenoid cavity is decreased. The long axis is thus parallel with that of the body instead of being transverse. In the placental mammals the coracoid, although developing independently, has dwindled to a beaklike process and fuses with and becomes part of the scapula. It does not articulate with the sternum.

      The clavicle is present generally in those placental mammals (primates, many rodents and marsupials, and others) that have prehensile (i.e., capable of grasping) forelimbs or whose forelimbs are adapted for flying (e.g., bats). In many mammals it is suppressed or reduced, as in cats, or absent, as in whales, sea cows, and hoofed animals.

pelvic girdle

      The pelvic girdle of the elasmobranch fishes (e.g., sharks, skates, and rays) consists of either a curved cartilaginous structure called the puboischial bar or a pair of bars lying transversely in the ventral part of the body anterior to the cloaca; projecting dorsally on each side is a so-called iliac process. Connected with the process is a basal cartilage. The basal cartilage carries a series of radialia, the skeleton of the paired pelvic fins. The pelvic girdles of many bony fishes are situated far forward, near the gills.

      There are marked variations in the form of the pelvic girdle in the amphibians (amphibian). In the frog the three parts of the hip bone (ilium, ischium, and pubis) are present. The pubic elements, however, remain wholly cartilaginous. The hip bone is characterized by the great length and forward extension of the ilium. The girdle is connected with the costal element of one vertebra, thus establishing a sacral region of the vertebral column. The acetabulum (the cup-shaped structure in which the femur articulates) is situated at the junction of the three elements.

      The pelvic girdle of some reptiles (reptile) has a loose connection with the spine. In most reptiles the ilium is joined to two sacral vertebrae. Both the pubic and the ischial parts usually meet in the so-called ventral symphysis, from which a cartilage or a bone, the hypoischium, projects backward to support the margin of the cloacal orifice, and another, the epipubis, projects forward. A few snakes (e.g., boas (boa)) retain vestiges of a pelvic girdle and limb skeleton.

      In most birds (bird) the ilium extends forward and backward and is fused with the many vertebrae, forming a synsacrum. The slender ischia and pubes do not form symphyses except in the ostrich.

      In most mammals (mammal) the ilium articulates with the sacrum, and the pubes meet in a symphysis anteriorly. A cotyloid bone, formed in the cartilage in the bottom of the acetabulum, is usually found. The symphysis pubis is not present in certain mammals (e.g., moles (mole)). In monotremes and marsupials (marsupial) the marsupial bones that support the pouch have been regarded as part of the epipubis.

Limbs

 The pectoral fin of the elasmobranchs possesses basal cartilages that articulate with the pectoral girdle. They carry a number of radial cartilages consisting of varying numbers of short segments; beyond these are located delicate fin rays.

      The proximal segment of the pelvic fin of sharks (shark) is supported by a single basal cartilage and by one or two radialia. In the pectoral fin of the primitive ray-finned fish Polypterus (bichir), three elements constitute the proximal segment of the fin: two bony rods, the propterygium and the metapterygium, on the margins and an intermediate partly ossified cartilage, the mesopterygium.

      The adoption of an upright position of the trunk, as seen in certain lemurs (lemur) and in the great apes (ape), has brought about further modification. In humans the lower limbs are used for bipedal locomotion, thus freeing the upper limbs for prehensile use. Many of the great apes have developed the use of the upper limb for an arboreal life; therefore, they are sometimes distinguished as brachiators (i.e., animals whose locomotion is by swinging with the arms from branches or other supports).

      The skeleton of the free limb of the land vertebrate is divisible into three segments: proximal, medial, and distal.

      The proximal segment consists of a single bone (the humerus in the forelimb, the femur in the hind limb). The humerus articulates by its rounded head with the glenoid cavity of the scapula and by condyles with the bones of the forearm. Its shaft is usually twisted and has ridges and tuberosities for the attachment of muscles.

      The femur is essentially cylindrical; the ends are expanded. At the proximal end, for articulation with the acetabulum, is the rounded head; near it are usually two elevations (trochanters) for muscle attachment. Three trochanters are characteristic of certain mammals (e.g., horse, rhinoceros). Distally, the femur expands into two condyles for articulation with the tibia. In many types there is an articular facet on the lateral surface for the head of the fibula.

      The medial segment of the limb typically contains two bones: the radius and the ulna in the forelimb and the tibia and the fibula in the hind limb. In the forelimb the radius is anterior, or preaxial (i.e., its position is forward to that of the ulna), in the adjustment of the limb for support and locomotion on land. Mammals in which the radius is fixed in pronation—i.e., in which the forelimb is rotated so that the shaft of the radius crosses in front of that of the ulna—are called pronograde. The radius transmits the weight of the forepart of the body to the forefeet, but it is the ulna that makes the elbow joint with the humerus; into its proximal end are inserted the flexor and extensor muscles of the forelimb.

      The tibia and fibula are separate in salamanders (salamander) and newts (newt), united in frogs (frog) and toads (toad). In land reptiles the tibia articulates with both condyles of the femur and with the tritibiale of the ankle. The fibula articulates with the postaxial femoral condyle and with the tritibiale and fibulare. The tibia of birds is long, the fibula reduced. In mammals the fibula is generally reduced and may be fused with the tibia and excluded from the knee joint.

      The distal segment of the limb comprises the carpus (wrist), metacarpus (metacarpal), and phalanges in the forelimb and the tarsus, metatarsus, and phalanges in the hind limb. A typical limb has five digits (fingers or toes), which contain the phalanges.

      The carpus and the tarsus of the higher vertebrates have probably been derived from a primitive structure by the fusion or suppression of certain of its elements. The bones of a generalized carpus (or tarsus) end in three transverse rows: a proximal row of three bones, the radiale (or tibiale), intermedium, and ulnare (or fibulare); a distal row of five carpalia (or tarsalia), numbered one to five from the radial (or tibial) margin; and an intermediate row of one or two centralia.

      In many urodele amphibians (e.g., salamanders), the carpus is generalized. In the frogs and toads, however, it is more specialized; only six carpals (carpal bone) are present, the third, fourth, and fifth carpalia probably having fused with either or both centralia. In birds the radiale and ulnare are distinct, but the distal bones are fused with the metacarpus to form a carpometacarpus. In mammals various examples of fusion and suppression occur. In humans the radiale forms the scaphoid bone; the intermedium forms the lunate bone; the ulnare forms the triquetral. The pisiform bone in humans is probably the remains of an extra digit. It may, however, be a sesamoid bone (i.e., an ossification within a tendon). The trapezium and trapezoid are carpalia 1 and 2; the capitate is derived from carpal 3; carpalia 4 and 5 have fused to form the hamate. An os centrale is present in the carpus of many monkeys (monkey). In mammals the number of digits varies, but the number of phalanges in each digit present usually corresponds with that of humans. In some species, however, the phalanges are more numerous, as when the limb is modified to form a paddle (e.g., in whales).

      The tarsus of urodele amphibians has the typical arrangement of bones. In the frogs and toads the intermedium is absent; two long bones are the tibiale and fibulare. Among the reptiles there is much variation in the composition of the tarsus. Generally, the joint of the ankle is intratarsal, the row of tarsalia being distal to the hinge. In most modern reptiles the tibiale and intermedium fuse to form the talus. In birds the ankle hinge is of the reptilian pattern in being intratarsal. The three tarsal cartilages of the embryo fuse to form the talus, which fuses with the tibia to form the tibiotarsus. The tarsalia fuse with the ends of the united metatarsals to make a tarsometatarsus. In the mammalian tarsus the talus is generally composed of the fused tibiale and intermedium, but in some a centrale is included to form a tritibiale. The ankle joint is not intratarsal but is located between the bones of the leg and the first row of tarsal bones, usually the tibia and the talus.

 Suppression of digits in hoofed mammals frequently has occurred in the following sequence: the pollex (first digit) is the first to be suppressed, then the minimus (fifth digit), the index (second digit), and finally the annularis (fourth digit). Among the even-toed ungulates (ungulate) (artiodactyls; e.g., the pig and the hippopotamus) the pollex has disappeared, and the other four digits are present, although the second and fifth digits are much reduced. In the camel only the third and fourth digits persist and are of equal importance. Among the odd-toed ungulates (perissodactyls; e.g., the horse) the right digit is dominant; the others are reduced to rudiments or splints.

Joints (joint)

      The junctions between the bony or cartilaginous units of vertebrate skeletons and between the body-wall ossicles of sea urchins (sea urchin) (Echinodermata) are often kept rigid by dovetailed margins. One skeletal unit, however, may move freely on another, as shown by the ambulacral ossicles along the arms of brittlestars, crinoids (crinoid), and starfishes (sea star) among the echinoderms and by the leg bones and vertebrae of vertebrates in which joints exist that permit various types of movement.

      Joints (joint) located between the bony or cartilaginous units of vertebrate skeletons are very simple in animals with a cartilaginous skeleton. When bone replaces cartilage, however, stronger and more-elaborate joints form. Flat, articulating, cartilaginous surfaces between the vertebral centra of sharks (shark) do not permit extensive movement, but it is sufficient for these animals. In sharks, intervertebral cones of notochord persist, with conical ends projecting into the ends of adjacent vertebrae. Joints between bones and cuticular sclerites may permit movement in one plane only, as in most arthropodan joints and the interphalangeal joint in humans.

      Between some bones (e.g., the human femur and pelvis) there is a ball-and-socket (ball-and-socket joint) device, by which a ball-like articular facet rotates in a concavity, known as the acetabulum. The femur is thus able to move in a variety of planes. The bony vertebrae of fishes, amphibians, reptiles, and birds possess centra articulating with one another in a ball-and-socket manner. The terrestrial animals strengthen the ball-and-socket articulation and sometimes restrict its movement by additional imbricating facets (zygapophyses). snake vertebrae interlock firmly with one another; a hemispherical posterior projection from each articulates with an anterior concavity (i.e., a cup-shaped depression) on the vertebra in front of it. The freely moving joints permit a twisting movement, with extra support being gained by two sets of sliding facets between each pair of consecutive vertebrae.

      Ball-and-socket joints, common in vertebrates, are easily contrived in animals with an endoskeleton. Among invertebrates are some remarkable parallels. In certain millipedes (millipede) (Juliformia), heavy circular sclerites encompass each segment and slightly overlap. Rotation of one skeletal ring upon the next, as well as flexion, is possible. The animal can thus curve its hard body in any direction. It can curl up dorsoventrally with the legs in the middle of a spiral and then walk with the legs on the ground and at right angles to the coiled position. Echinoderms also possess many ball-and-socket joints, such as those located at the base of spines in sea urchins.

      Various types of strong hinge joints, easily contrived by an arthropod, also occur in vertebrates. The joint between the skull and the first vertebra in mammals is a strong hinge. A pair of occipital condyles on the skull that articulate against shallow concavities on the anterior face of the vertebra permits a nodding movement of the head. The strongest hinge joints in arthropods also bear a double articulation, as in the leg of the spider and in Scutigera, the fastest-running centipede. Hinge joints in vertebrates are often composite, being formed or supported by the incorporation of several small bones, as in the human wrist. To facilitate cursorial, or running, habits, flexion is limited to one plane.

      In contrast, a series of small bones at the wrist or ankle can provide a marked flexibility in many directions, in addition to strength. A leg that can flex in various directions is usually achieved in arthropods by a series of pivot joints. Each joint is set in a different plane along the leg in such a way that the combined action of the several joints enables the leg to move in any direction. Single endoskeletal joints of vertebrates supply a variety of movements with greater ease; no duplication is necessary.

      In vertebrates the joints between bones are constructed in a variety of ways. They fall, however, into two main categories, the synovial joint and the nonsynovial joint. In the former, known also as diarthrosis, a cleft occurs between the free surfaces of two skeletal parts; during movements these surfaces slide on each other. In the nonsynovial type, known also as synarthrosis, the skeletal parts are connected by nonosseous material that permits bending or twisting. The range of movement is greater in the synovial than in the nonsynovial type. In the course of vertebrate evolution, the nonsynovial type appears to have preceded the synovial. The latter is unusual in fishes, but the majority of the joints in humans and other mammals are of this form. The amphiarthrosis is an intermediate type of joint in humans. In this type the connecting material between the bones contains a cavity, but movement depends on bending of the connecting material.

      Some of the strongest movements in arthropods (e.g., in the legs of Polydesmida, an order of millipedes) are also implemented by a joint that possesses cavities containing synovial fluid in which imbricating cuticular facets slide against one another. Levers exist in vertebrates in the heel bone and in the human elbow projection (olecranon process).

      Movements at joints are commonly produced by voluntary muscular action. Such movements are distinguished as “active”; movements produced by the application of external force, whether by manipulation or by the energy of moving parts or gravity, are known as “passive.”

      Muscles may be situated in such a way that they can act on only one joint (uniarticular muscles), but many muscles can act on two or more joints (bi- and multiarticular muscles). A multiarticular muscle will act on only one joint if the remaining joints under its control are fixed by other muscles. Muscles, however, rarely contract as isolated units. They usually act as a group; this phenomenon is known as the “group action of muscles.” The intricate adjustment and coordination of muscular tensions that are required for posture and movement fall under the control of the central nervous system.

      Although the general form of the skeleton is hereditary, it is also influenced by mechanical factors, such as pressure on the cartilage at the end of a bone (epiphysis) or stresses applied to the external surface (e.g., from adjacent muscles). The effect of pressure on bone depends on whether the bony surface is covered by periosteum or by cartilage. In the case of the periosteum, which has blood vessels, pressure causes impairment of blood supply and absorption of underlying bone. On the other hand, pressure on cartilage, which has no blood supply, does not cause absorption. Internal strains stimulate bone formation, and, when the direction of stress is altered, bony reconstruction takes place.

      When a bone is fractured (fracture), some bone tissue adjacent to the fracture is absorbed, and a mass of tissue termed callus, at first uncalcified, makes its appearance between and around the broken ends. Cartilage formation commonly takes place in the callus even when the fracture is in a membrane bone (e.g., the parietal bone of the skull). Callus also contains osteoblasts (osteoblast) derived from both periosteum and endosteum, the connective tissue within a bone. The formation of callus is greater if there is pressure and movement between the broken ends of the bone and is most pronounced on the concave side when the bony fragments are at an angle. Bony union is effected by calcification and subsequent ossification of the callus. Regeneration of bone is more active in the shafts of long bones, the lower jaw, and the ribs than in the skull and the spongy ends of long bones.

William James Hamilton Ed.

Additional Reading

R.B. Clark, Dynamics in Metazoan Evolution (1964), deals with some aspects of the coelomate condition, hydrostatic skeletons, metamerism, and their evolution. J. Gray, Animal Locomotion (1968), a comprehensive, comparative account of the coordination and mechanisms of vertebrate locomotion, with some chapters on invertebrates (the approach is for the nonspecialist, but the treatment is mathematical and neurological); A.S. Romer, The Vertebrate Body, 4th ed. (1970), an excellent account of the evolution of the skeleton in vertebrates; and J.Z. Young, The Life of Vertebrates, 2nd ed. (1962).

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