Integument PDF

kar24239_ch06_212-239.qxd 12/22/10 3:41 PM Page 212 C H A P T E R 6 Integument E MBRYONIC O RIGIN...

kar24239_ch06_212-239.qxd 12/22/10 3:41 PM Page 212 C H A P T E R 6 Integument E MBRYONIC O RIGIN S PECIALIZATIONS OF THE I NTEGUMENT Nails, Claws, Hooves G ENERAL F EATURES OF THE I NTEGUMENT Horns and Antlers Dermis Baleen Epidermis Scales P HYLOGENY Dermal Armor Integument of Fishes Mucus Primitive Fishes Color Chondrichthyes O VERVIEW Bony Fishes Integument of Tetrapods Amphibians Reptiles Birds Mammals The integument (or skin) is a composite organ. On the sur- of embryonic development, then, epidermis and dermis are face is the epidermis, below it is the dermis, and between tightly coupled and mutually necessary. them lies the basement membrane (basal lamina and retic- As the critical border between the organism and its ular lamina). The epidermis is derived from the ectoderm exterior environment, the integument has a variety of spe- and produces the basal lamina (figure 6.1a). The dermis cialized functions. It forms part of the exoskeleton and thick- develops from mesoderm and mesenchyme and produces the ens to resist mechanical injury. The barrier it establishes reticular lamina. Between the integument and deep body prevents the entrance of pathogens. Skin swabs from healthy musculature is a transitional subcutaneous region made up of human volunteers identified over 200 different genera of res- very loose connective and adipose tissues. In microscopic ident bacteria, including many that, if given the chance examination, this region is termed the hypodermis. In gross through a breach in the skin, would produce serious staph anatomical dissection, the hypodermis is referred to as the infections, acne, and eczema, among other pathologies. The superficial fascia (figure 6.1b). integument helps hold the shape of an organism as well. The integument is one of the largest organs of the body, Osmotic regulation and movement of gases and ions to and making up some 15% of the human body weight. Epidermis and from the circulation are aided by the integument in conjunc- dermis together form some of the most varied structures found tion with other systems. Skin gathers needed heat, or radiates within vertebrates. The epidermis produces hair, feathers, the excess, and houses sensory receptors. It holds feathers for baleen, claws, nails, horns, beaks, and some types of scales. The locomotion, hair for insulation, and horns for defense. Skin dermis gives rise to dermal bones and osteoderms of reptiles. pigments block harmful sunlight and display bright colors dur- Collectively, epidermis and dermis form teeth, denticles, and ing courtship. The list of functions can easily be extended. scales of fish. In fact, the developmental destinies of dermis and The remarkable variety of skin structures and roles epidermis are so closely linked across the basement membrane makes it difficult to briefly summarize the forms and functions that in the absence of one, the other by itself is incapable of or of the integument. Let us begin by examining the embryonic inhibited from producing these specialized structures. In terms origin and development of the skin. 212  Dermatome Myotome Somite Sclerotome Epidermis Basement membrane Dermis Ectoderm Neural crest cell Hypodermis (migrating to dermis) Sensory Endocrine Exocrine Interaction Dermatome Periderm FIGURE 6.2 Specializations of the integument. Myotome Stratum basale Sensory receptors reside in the skin. Exocrine glands with ducts Basal lamina and ductless endocrine glands form from invaginations of the (a) epidermis.Through a dermal-epidermal interaction, specialized Mucous cuticle skin structures such as hair, feathers, and teeth arise. Epidermis Basal lamina Basement membrane Dermis distinct dermatome that differentiates into the connective Chromatophore tissue component of the dermis. Connective tissue within Stratum Hypodermis the skin is usually diffuse and irregular, although in some compactum species collagen bundles are arranged into a distinct, ordered layer within the dermis. This layer is called the stratum com- (b) pactum (figure 6.1b). Cells of neural crest origin migrate into FIGURE 6.1 Embryonic development of the skin. the region between dermis and epidermis, contributing to (a) Cross section of a representative vertebrate embryo.The bony armor and to skin pigment cells called chromatophores ectoderm initially differentiates into a deep stratum basale, which (meaning “color” and “bearing”). Usually chromatophores replenishes the outer periderm.The dermatome settles in under reside in the dermis, although in some species they may send the epidermis to differentiate into the connective tissue layer of pseudopods into the epidermis or take up residence there dermis. As migrating neural crest cells pass between dermis and themselves. Often, chromatophores are scattered within the epidermis, some settle between these layers to become the hypodermis. Nerves and blood vessels invade the integument chromatophores. (b) The epidermis further differentiates into a to round out its structural composition. stratified layer that often has a mucous coat or cuticle on the Fundamentally, the integument is composed of two surface.Within the dermis, collagen forms distinctive plies (layers) layers, epidermis and dermis, separated by the basement that constitute the stratum compactum.The basement membrane membrane. Vascularization and innervation are added, lies between the epidermis and the dermis. Beneath the dermis and the deeper layer of musculature is the hypodermis, a along with contributions from the neural crest. From such collection of loose connective and adipose tissues. simple structural ingredients, a great variety of integumen- tary derivatives arises. The integument houses sensory organs that detect arriving stimuli from the external environment. Invagination of the surface epidermis forms skin glands: Embryonic Origin exocrine if they retain ducts, and endocrine if they separate from the surface and release products directly into blood ves- By the end of neurulation in the embryo, most skin precur- sels (figure 6.2). Interaction between epidermis and dermis sors are delineated. The single-layered surface ectoderm pro- stimulates specializations such as teeth, feathers, hair, and liferates to give rise to the multilayered epidermis. The deep scales of several varieties (figure 6.3a–i). layer of the epidermis, the stratum basale (stratum germina- tivum), rests upon the basement membrane. Through active cell division, the stratum germinativum replenishes the sin- General Features of the Integument gle layer of outer cells called the periderm (figure 6.1a). Additional skin layers are derived from these two as differen- Dermis tiation proceeds. The dermis of many vertebrates produces plates of bone The dermis arises from several sources, principally from directly through intramembranous ossification. Because of the dermatome. The segmental epimeres (somites) divide, their embryonic source and initial position within the der- producing the sclerotome medially, the embryonic source of mis, these bones are called dermal bones. They are promi- the vertebrae, and the dermomyotome laterally. Inner cells nent in ostracoderm fishes but appear secondarily even in of the dermomyotome become rearranged into the myotome, derived groups, such as in some species of mammals. the major source of skeletal muscle. The outer wall of the der- momyotome spreads out under the ectoderm as a more or less Dermal (intramembranous) bone development (p. 184) Integument 213 kar24239_ch06_212-239.qxd 12/22/10 3:41 PM Page 214 (b) Bird feather (c) Mammalian hair (a) Generalized development 8 7 1 7 8 6 6 5 5 2 4 4 3 (d) Mammary 4 4 gland 5 4 5 6 6 7 7 5 5 8 8 6 6 9 7 7 7 (e) Vertebrate tooth 8 8 8 8 (f) Placoid scale (g) Cosmoid scale (h) Ganoid scale (i) Cycloid-ctenoid scale FIGURE 6.3 Skin derivatives. (a) Out of the simple arrangement of epidermis and dermis, with a basement membrane between them, a great variety of vertebrate integuments develops. Interaction of epidermis and dermis gives rise to feathers in birds (b), hair and mammary glands in mammals (c and d), teeth in vertebrates (e), placoid scales in chondrichthyans (f), and cosmoid, ganoid, and cycloid- ctenoid scales in bony fishes (g–i). Based on the research of Richard J. Krejsa in Wake. The most conspicuous component of the dermis is considerably (figure 6.5a,b). This principle seems to gov- the fibrous connective tissue composed mostly of collagen ern the tightly woven collagen of shark skin. Its flexible fibers. Collagen fibers may be woven into distinct layers skin bias accommodates lateral bending of the body but called plies. The dermis of the protochordate amphioxus simultaneously resists distortions in body shape. As a exhibits an especially ordered arrangement of collagen result, the skin stretches without wrinkling. Because it does within each ply (figure 6.4). In turn, plies are laminated not wrinkle, water flows smoothly and without turbulence together in very regular, but alternating, orientation. across the surface of the body (figure 6.5d). These alternating layers act like warp and weft threads of In fishes and aquatic vertebrates, including cetaceans cloth fabric, giving some shape to the skin and preventing and aquatic squamates, collagen fibers of the dermis are usu- it from sagging. In aquatic vertebrates, such as sharks, the ally arranged in orderly plies that form a recognizable stra- bundles of collagen lie at angles to each other, giving the tum compactum. In terrestrial vertebrates, the stratum skin a bias, like cloth; that is, the skin stretches when it is compactum is less obvious because locomotion on land pulled at an angle oblique to the direction of the bundles. depends more on the limbs and less on the trunk. And, of For example, if you take a piece of cloth, like a handker- course, any wrinkling of the skin is less disruptive to a ter- chief, and pull it along either warp or weft threads, the restrial vertebrate moving through air. Consequently, colla- cloth extends very little under this parallel tension. But if gen fibers are present, even abundant, in the skin of you pull at opposite corners, tension is applied obliquely terrestrial vertebrates, but they are much less regularly at a 45° angle to the threads, and the cloth stretches ordered and usually do not form distinct plies. 214 Chapter Six  Mucous surface layer (a) (b) Epidermis Basal (c) lamina Dermis Fibrocyte layer Loose connective tissue FIGURE 6.4 Protochordate, skin of amphioxus. The 45° epidermis is a single layer of cuboidal or columnar cells that secrete a mucus that coats the surface and rests upon a basal 90° lamina.The dermis consists of very highly ordered collagen fibers Body arranged in alternating plies (layers) to form a “fabric” that brings axis structural support as well as flexibility to the outer body wall. Pigment is secreted by the epidermal cells themselves. After Olsson. (d) 45° FIGURE 6.5 Bias in woven material. (a) Warp Epidermis (longitudinal threads) and weft (cross threads) compose the The epidermis of many vertebrates produces mucus to moisten fibers of fabric. If the tensile force is parallel with the threads the surface of the skin. In fishes, mucus seems to afford some (indicated by the arrows), little distortion of the fabric occurs. protection from bacterial infection and helps ensure the lami- (b) However, tension along the bias at 45° to the threads results in a substantial change in shape. (c) Fashion designers take nar flow of water across the body surface. In amphibians, advantage of these features of fabric when designing clothes. In mucus probably serves similar functions and additionally keeps the loose bias direction, the fabric falls into folds and pleats but the skin from drying during the animal’s sojourns on land. can hold its shape along the warp-and-weft threads. (d) Plies of In terrestrial vertebrates, the epidermis covering the body collagen of the stratum compactum of fish skin act in a similar often forms an outer keratinized or cornified layer, the stratum way.The flexible bias of the skin is oriented at 45° to the body corneum. It is one of the tetrapod innovations that help them length, thus accommodating lateral bending during swimming.This address life in a drying and abrasive terrestrial environment. arrangement keeps the skin flexible but tight so that surface All cells in the stratum corrneum are dead cells. New wrinkling does not occur and turbulence is not induced in the epidermal cells are formed by mitotic division, primarily in the streamlines passing over the body as the fish swims. deep stratum basale. These new epidermal cells push more After Gordon. superficial ones toward the surface, where they tend to self- destruct in an orderly fashion. During their demise, various pro- corneum is a nonliving layer that serves to reduce water loss tein products accumulate and collectively form keratin in a through the skin in dry terrestrial environments. Keratin is a process called keratinization. The resulting superficial stratum class of proteins produced during keratinization, and the specific Integument 215  Callus Epidermal cell Granular cell Epidermis Club cell Cutaneous pigment Dermis Stratum corneum Nerve fiber Deep pigment layer Subcutaneous S. lucidum tissue E S. granulosum Muscle S. spinosum FIGURE 6.7 Lamprey skin. Among the numerous S. basale epidermal cells are separate unicellular glands, the granular cells D and the club cells. Note the absence of keratinization.The dermis consists of regularly arranged collagen and chromatophores. FIGURE 6.6 Keratinization. In places where mechan- ical friction increases, the integument responds by increasing some herbivorous minnows, and the friction surface on the production of a protective keratinized callus, and the stratum belly skin of some semiterrestrial fish are all keratinized corneum thickens as a result. Key: E, epidermis; D, dermis. derivatives. However, in most living fishes, the epidermis is alive and active on the body surface, and there is no promi- nent superficial layer of dead, keratinized cells. Surface cells epidermal cells that participate are keratinocytes. In saurop- are often patterned with tiny microridges that perhaps hold sids, the epidermis produces two types of keratinocytes—one the surface layer of mucus. The mucous layer is formed from type containing alpha (soft) and the other beta (hard) forms of various individual cells in the epidermis with contributions keratin. Alpha-keratins are present in most flexible epider- from multicellular glands. This mucous coat, termed a mal layers where shape changes occur. Beta-keratins are more mucous cuticle, resists penetration by infectious bacteria, common in specializations such as hard scales, claws, beak, probably contributes to laminar flow of water across the sur- and feathers. In synapsids, only alpha-keratins are present. face, makes the fish slippery to predators, and often includes Keratinization and formation of a stratum corneum chemicals that are repugnant, alarming, or toxic to enemies. also occur where friction or direct mechanical abrasion Two types of cells occur within the epidermis of fishes: insult the epithelium. For example, the epidermis in the oral epidermal cells and specialized unicellular glands. In living cavity of aquatic and terrestrial vertebrates often exhibits a fishes, including cyclostomes, prevalent epidermal cells keratinized layer, especially if the food eaten is unusually make up the stratified epidermis. Superficial epidermal cells sharp or abrasive. In areas of the body where friction is com- are tightly connected through cell junctions and contain mon, such as the soles of the feet or palms of the hands, the numerous secretory vesicles that are released to the surface cornified layer may form a thick protective layer, or callus, where they contribute to the mucous cuticle. Epidermal cells to prevent mechanical damage (figure 6.6). The stratum of the basal layer are cuboidal or columnar. Mitotic activity corneum may be differentiated into hair, hooves, horn is present in but not restricted to the basal layer. sheathes, or other specialized cornified structures. The term Unicellular glands are single, specialized, and inter- keratinizing system refers to the elaborate interaction of spersed among the epidermal cell population. There are epidermis and dermis that produces the orderly transforma- several types of unicellular glands. The club cell is an elon- tion of keratinocytes into such cornified structures. gate, sometimes binucleate, unicellular gland (figure 6.7). Finally, scales form within the integument of many Some chemicals within club cells excite alarm or fear. They aquatic and terrestrial vertebrates. Scales are basically folds in are thought to be released by observant individuals to warn the integument. If dermal contributions predominate, espe- others of imminent danger. The granular cell is a diverse cell cially in the form of ossified dermal bone, the fold is termed a found in the skin of lampreys and other fishes (figure 6.7). dermal scale. An epidermal fold, especially in the form of a Both granular and club cells contribute to the mucous cuti- thickened keratinized layer, produces an epidermal scale. cle, but their other functions are not fully understood. The goblet cell is a type of unicellular gland that is absent from lamprey skin but is usually found in other bony and carti- Phylogeny laginous fishes. It too contributes to the mucous cuticle and is recognized by its “goblet” shape, namely, a narrowed Integument of Fishes basal stem and wide apical end holding secretions. The elec- With few exceptions, the skin of most living fishes is tron microscope has helped distinguish an additional type nonkeratinized and covered instead by mucus. Exceptions of unicellular gland in the epidermis, the sacciform cell. include keratinized specializations in a few groups: The It holds a large, membrane-bound secretory product that “teeth” lining the oral disk of lampreys, the jaw coverings of seems to function as a repellent or toxin against enemies 216 Chapter Six once it is released. As increased attention is given to the Dentin Enamel Tubercles study of fish skin, other cell types are being recognized. This Pulp cavity growing list of specialized cells within the epidermis reveals Dermal bone a complexity and variety of functions that were not previ- Vascular ously appreciated. Collagen within the stratum compactum is regularly Lamellar organized into plies that spiral around the body of the fish, allowing the skin to bend without wrinkling. In some fishes, the dermis has elastic properties. When a swimming fish bends 0.2 mm its body, the skin on the stretched side stores energy that helps FIGURE 6.8 Section through an enlarged unbend the body and sweeps the tail in the opposite direction. ostracoderm scale. The surface consists of raised tubercles The fish dermis often gives rise to dermal bone, and capped with dentin and enamel enclosing a pulp cavity within. dermal bone gives rise to dermal scales. In addition, the sur- These tubercles rest upon a foundation of dermal bone, part of face of fish scales is sometimes coated with a hard, acellular the dermal armor covering the body. enamel of epidermal origin and a deeper dentin layer of der- After Kiaer. mal origin. Until recently, both enamel and dentin were rec- ognized on the basis of appearance, not on their chemical composition. As the surface appearance of scales changed between fish groups, so did the terminology. Enamel was Spine thought to give way phylogenetically to “ganoin” and dentin Enamel to “cosmine.” These terms were inspired by the superficial Basal Dentin plate appearance of scales, not by their chemical composition nor even by their histological organization. Perhaps it is best to (a) think of ganoin as a different morphological expression of Epidermal cell Epidermis enamel, and cosmine as a different morphological expres- Secretory cell Dermis sion of dentin and to be prepared for subtle chemical differ- ences as we meet them. (b) Pulp cavity Primitive Fishes In ostracoderms and placoderms, the integument produced Chromatophore prominent bony plates of dermal armor that encased their bodies in an exoskeleton. Dermal bones of the cranial FIGURE 6.9 Shark skin. (a) Surface view of the skin region were large, forming the head shields; but more pos- showing regular arrangement of projecting placoid scales. teriorly along the body, the dermal bones tended to be bro- (b) Section through a placoid scale of a shark.The projecting ken up into smaller pieces, the dermal scales. The surface scale consists of enamel and dentin around a pulp cavity. of these scales was often ornamented with tiny, mushroom- shaped tubercles. These tubercles consisted of a surface layer of enamel or an enamel-like substance over an inner layer of dentin (figure 6.8). One or several radiating pulp Chondrichthyes cavities resided within each tubercle. The dermal bone In cartilaginous fishes, dermal bone is absent, but surface den- supporting these tubercles was lamellar, organized in a lay- ticles, termed placoid scales, persist. These scales are what ered pattern. give the rough feel to the surface of the skin (figure 6.9a). The skin of living hagfishes and lampreys departs con- Recent evidence suggests that these tiny placoid scales favor- siderably from that of primitive fossil fishes. Dermal bone is ably affect the water flowing across the skin as the fish swims absent, and the skin surface is smooth and without scales. forward to reduce friction drag. Numerous secretory cells are The epidermis is composed of stacked layers of numerous liv- present in the epidermis as well as stratified epidermal cells. ing epidermal cells throughout. Interspersed among them The dermis is composed of fibrous connective tissue, espe- are unicellular glands, namely, the large granular cells and cially elastic and collagen fibers, whose regular arrangement elongate club cells. In addition, the skin of hagfishes forms a fabriclike warp and weft in the dermis (figure 6.5d). includes thread cells that discharge thick cords of mucus to This gives the skin strength and prevents wrinkling during the skin surface when the fish is irritated. The dermis is swimming. highly organized into regular layers of fibrous connective tis- The placoid scale itself develops in the dermis but sue. Pigment cells occur throughout the dermis. The hypo- projects through the epidermis to reach the surface. A cap of dermis includes adipose tissue. Within the dermis, hagfishes enamel forms the tip, dentin lies beneath, and a pulp cavity also possess multicellular slime glands that release their resides within (figure 6.9a,b). Chromatophores occur in the products via ducts to the surface. lower part of the epidermis and upper regions of the dermis. Integument 217 kar24239_ch06_212-239.qxd 12/22/10 3:42 PM Page 218 B O X E S S AY 6. 1 Poison Darts and Poison Frogs The skin of most amphibians contains glands that secrete products that are dis- tasteful or even toxic to predators. Often these skin toxins are not manufactured by the frogs themselves, but instead are co-opted from toxins in their prey, such as from ants or other arthropods. Some ant specialists suggest that the insects, in turn, may get the toxins or toxin precursors from their diet. In tropical regions of the BOX FIGURE 1 Poison dart frog. New World lives a group of frogs, the poi- Its bright colors advertise toxic skin secretions son dart frogs, with especially toxic skin that are poisonous to most predators. secretions (box figure 1). Native peoples of the region often gather these frogs, hold their darts. Game shot with these toxin- by future research, the toxins these native them on sticks over a fire to stimulate laced darts is quickly tranquilized or killed. peoples use would travel the ecological release of these secretions, and then Cooking denatures the toxins, making the web back, through frogs, to insects, to collect the secretions on the tips of game safe for humans to eat. If confirmed their diet. Bony Fishes The dermis of bony fishes is subdivided into a superficial layer of loose connective tissue and a deeper layer of dense fibrous connective tissue. Chromatophores are found within the dermis. The most important structural product of the dermis is the scale. In bony fishes, dermal scales do Dermal scale not actually pierce the epidermis, but they are so close to Epidermis the surface they give the impression that the skin is hard (figure 6.10a,b). The epidermal covering includes a basal layer of cells. Above this layer are stratified epidermal cells. As they move toward the surface, epidermal cells undergo (a) cytoplasmic transformation, but they do not become kera- tinized. Within these layered epidermal cells occur single unicellular glands, the secretory and club cells. These uni- cellular glands, along with epidermal cells, are the source Mucous cuticle of the mucous cuticle, or surface “slime.” On the basis of their appearance, several types of scales are recognized among bony fishes. The cosmoid scale, seen in primitive sarcopterygians, resides upon a double layer of bone, one layer of which is vascular and the Epidermal cell other lamellar. On the outer surface of this bone is a layer that is now generally recognized as dentin, and spread superficially on the dentin is a layer now recognized as Club cell enamel. The unusual appearance of these enamel and dentin coats inspired, in the older literature, the respective Basal layer names of “ganoin” and “cosmine,” on the mistaken belief that ganoin was fundamentally a different mineral from (b) enamel and cosmine different from dentin. Although the chemical nature of these layers is now clear, the earlier FIGURE 6.10 Bony-fish skin. (a) Arrangement of names have stuck to give us the terms for distinctive scale dermal scales within the skin of a teleost fish (arrows indicate types. In the cosmoid scale, there is a thick, well-developed direction of scale growth). (b) Enlargement of epidermis. Note layer of dentin (cosmine) beneath a thin layer of enamel epidermal cells and club cells. (figure 6.11a). (a) After Spearman. 218 Chapter Six  Enamel Integument of Tetrapods Dentin (cosmine) Vascular bone Although keratinization occurs in fishes, among terrestrial Bone Bone Lamellar bone vertebrates it becomes a major feature of the integument. Extensive keratinization produces a prominent outer corni- (a) Cosmoid scale fied layer, the stratum corneum, that resists mechanical abrasion. Lipids are often added during the process of kera- Enamel tinization or spread across the surface from specialized (ganoin) Vascular bone glands. The cornified layer along with these lipids increases Bone Lamellar bone the resistance of the tetrapod skin to desiccation. Multicellular glands are more common in the skin of Palaeoniscoids Ancestral actinopterygian tetrapods than in the skin of fishes. In fishes, the mucous (b) Ganoid scale cuticle and secretions of the unicellular glands at or near the surface of the skin coat it. In contrast, among tetrapods, mul- ticellular glands usually reside in the dermis and reach the surface through common ducts that pierce the cornified Bone layer. Thus, the stratum corneum that protects the skin and (c) Teleost scale prevents desiccation also controls the release of secretions directly to the surface. If it were not for these openings in the stratum corneum, the surface of the skin could not be coated or lubricated by these secretions. (d) Cycloid Ctenoid Amphibians Amphibians are of special interest because during their lives FIGURE 6.11 Scale types of bony fishes. Cross they usually metamorphose from an aquatic form to a terres- section of a cosmoid scale (a), a ganoid scale (b), and a teleost trial form. In most modern amphibians, the skin is also spe- scale (c). Surface views of the two types of the teleost scale, cialized as a respiratory surface across which gas exchange cycloid and ctenoid scales (d). occurs, with the capillary beds in the lower epidermis and deeper dermis. In fact, some salamanders lack lungs and depend entirely on cutaneous respiration through the skin to meet their metabolic needs. Cutaneous respiration (p. 417) The ganoid scale is characterized by the prevalence of a thick surface coat of enamel (ganoin), without an The most primitive tetrapods had scales like the underlying layer of dentin (figure 6.11b). Dermal bone fishes from which they arose. Among living amphibians, forms the foundation of the ganoid scale, appearing as a dermal scales are present only as vestiges in some species of double layer of vascular and lamellar bone (in palaeonis- tropical caecilians (Apoda). Frogs and salamanders lack all coid fishes) or a single layer of lamellar bone (in other traces of dermal scales (figure 6.12a). In salamanders, the ancestral actinopterygians). Ganoid scales are shiny skin of the aquatic larvae includes a dermis of fibrous con- (because of the enamel), overlapping, and interlocking. nective tissue, consisting of superficial loose tissue over a Living polypteriforms and gars retain ganoid scales. How- compact deep layer. Within the epidermis are deep basal ever, in most other lines of bony fishes, ganoid scales are cells and surface apical cells. Scattered throughout are reduced through the loss of the vascular layer of bone and large Leydig cells thought to secrete substances that resist loss of the enamel surface. This produces, in teleosts, a entry of bacteria or viruses (figure 6.12b). In terrestrial rather distinctive scale. adults, the dermis is similarly composed of fibrous connec- The teleost scale lacks enamel, dentin, and a vascular tive tissue. In the epidermis, Leydig cells are now absent, bone layer. Only lamellar bone remains, which is acellular and but distinct regions can be recognized, such as the strata mostly noncalcified (figure 6.11c). Two kinds of teleost scales basale, spinosum, granulosum, and corneum. Presence of are recognized. One is the cycloid scale, composed of con- a thin stratum corneum affords some protection from centric rings, or circuli. The other is the ctenoid scale, with a mechanical abrasion and retards loss of moisture from the fringe of projections along its posterior margin (figure 6.11d). body without unduly shutting off cutaneous gas exchange. New circuli are laid down, like rings in a tree, as a teleost fish During the breeding season, nuptial pads may form on dig- grows. Annual cycles are evident in the groupings of these cir- its or limbs of male salamanders or frogs. Nuptial pads are culi, and from this pattern in the scales we can determine the raised calluses of cornified epidermis that help the male age of individual fish. hold the female during mating. Integument 219  Epidermis Stratum corneum Generally, the skin of frogs and salamanders includes Transitional layer Chromatophores Poison gland two types of multicellular glands: mucous and poison glands. Stratum germinativum Both are located in the dermis and open to the surface through connecting ducts (figure 6.12b). The mucous glands tend to be smaller, each being made up of a little cluster of cells that Mucus release their product into a common duct. The poison glands Dermis gland (granular glands) tend to be larger and often contain stored secretions within the lumen of each gland. Secretions of poison glands tend to be distasteful or even toxic to predators. How- ever, few persons handling amphibians are bothered by this Muscle secretion, nor need they be concerned, because it is potentially harmful only if eaten or injected into the bloodstream. Chromatophores may occasionally be found in the amphibian epidermis, but most reside in the dermis. Capil- lary beds, restricted to the dermis in most vertebrates, reach (a) into the lower part of the epidermis in amphibians, a feature serving cutaneous respiration. Stratum Leydig cell corneum Reptiles Transitional The skin of reptiles reflects their greater commitment to a layer Epidermis terrestrial existence. Keratinization is much more extensive, Stratum and skin glands are fewer than in amphibians. Scales are basale Chromatophore present, but these are fundamentally different from the der- Mucous Poison mal scales of fishes, which are built around bone of dermal gland Dermis gland origin. The reptilian scale usually lacks the bony undersup- port or any significant structural contribution from the der- mis. Instead, it is a fold in the surface epidermis, hence, an epidermal scale. The junction between adjacent epidermal (b) scales is the flexible hinge (figure 6.13a). If the epidermal scale is large and platelike, it is sometimes termed a scute. FIGURE 6.12 Amphibian skin. (a) Section through an adult frog skin.A basal stratum basale and a thin, superficial Additionally, epidermal scales may be modified into crests, stratum corneum are present.The transitional layer between spines, or hornlike processes. them includes a stratum spinosum and a stratum granulosum. Although not usually associated with scales, dermal (b) Diagrammatic view of amphibian skin showing mucous and bone is present in many reptiles. The gastralia, a collection poison glands that empty their secretions through short ducts to of bones in the abdominal area, are examples. Where dermal the surface of the epidermis. bones support the epidermis, they are called osteoderms, Layers: Outer Hinge Inner Hinge Epidermis Dermis Basal Rest Renewel Shed Rest (a) (b) FIGURE 6.13 Reptile skin. (a) Epidermal scales. Extent of projection and overlap of epidermal scales varies among reptiles and even along the body of the same individual. Snake body scales (top) and tubercular scales of many lizards (bottom) are illustrated. Between scales is a thinned area of epidermis, a “hinge” allowing skin flexibility. (b) Skin shedding. Just before the old outer layer of epidermis is shed, the basal cells produce an inner epidermal generation.White blood cells collect in the splitting zone to promote separation of new from old outer epidermis. (a) After Maderson; (b) after Landmann. 220 Chapter Six  B O X E S S AY 6. 2 Borrowed Toxins The Asian snake, Rhabdophis tigrinus, pro- visions its defenses with toxins garnered from the natural prey it consumes, a poi- sonous toad. This toad possesses skin glands toxic to most vertebrates, but this snake, the tiger keelback snake, can toler- ate these toxins. In fact, upon digestion of the toad, the snake harvests these toxins to be redeployed in special nuchal (neck) glands.When the snake is bitten by its own predator, these glands on the snake’s neck burst, releasing the toxic contents that produce a burning distaste or even blind- ness if squirted into the eyes, thereby discouraging or deterring the attacker. There is even some evidence that female snakes can pass the toxins to their young embryos, equipping the youngsters with a ready defensive chemical arsenal when born. Sequestering toxins in inverte- brates is well known, but this discovery in BOX FIGURE 1 Tiger keelback snake and the Japanese toad, its toxic R. tigrinus may lead to discovery of similar prey. Note the raised keel (arrows) in the neck of this brightly colored snake, where are systems in other snakes feeding on stored the toxins gathered from the poisonous toad Bufo japonicus (inset), which it has amphibians with poisonous skin glands. eaten and digested. Photos kindly supplied by Deborah A. Hutchinson and Alan H. Savitzky, part of the research team including A. Mori, J. Meinwald, F. C. Schroeder, and G. M. Burghardt. plates of dermal bone located under the epidermal scales. jaw. In some turtles, scent glands can produce quite pungent Osteoderms are found in crocodilians, some lizards, and odors, especially when the animal is alarmed by handling. some extinct reptiles. Some bones of the turtle shell are Most integumental glands of reptiles are thought to play a probably modified osteoderms. role in reproductive behavior or to discourage predators, but The dermis of reptilian skin is composed of fibrous con- the glands and their social roles are not well understood. nective tissue. The epidermis is generally delineated into three regions: stratum basale, stratum granulosum, and stratum corneum. However, this changes prior to molting in those rep- Birds tiles that slough large pieces of the cornified skin layer. In tur- Basic Structure The feathers of birds have been called tles and crocodiles, sloughing of skin is modest, comparable to nothing more than elaborate reptilian scales. This oversim- birds and mammals, in whom small flakes fall off at irregular plifies the homology. Certainly the presence of epidermal intervals. But in lizards, and especially in snakes, shedding of scales along the legs and feet (figure 6.14a) of birds testifies the cornified layer, termed molting or ecdysis, results in to their debt to reptiles. If not a direct remodeled reptilian removal of extensive sections of superficial epidermis. As molt- scale, then the feather is as example of yet another more ing begins, the stratum basale, which has given rise to the strata fundamental homology of the underlying interaction of the granulosum (inner) and corneum (outer), duplicates the deeper epidermal-dermal layers producing such a skin specialization layers of granulosum and corneum, pushing up under the old (see figure 6.3). layers. White blood cells invade the stratum intermedium, a The dermis of bird skin, especially near the feather temporary layer between old and new skin (figure 6.13b). follicles, is richly supplied with blood vessels, sensory nerve These white blood cells are thought to promote the separation endings, and smooth muscles. During the brooding season, and loss of the old superficial layer of the skin. the dermis in the breast of some birds becomes increasingly Integumental glands of reptiles are usually restricted to vascularized, forming a brood patch in which warm blood certain areas of the body. Many lizards possess rows of femoral can come into close association with incubated eggs. glands along the underside of the hindlimb in the thigh The epidermis comprises the stratum basale and the region. Crocodiles and some turtles have scent glands. In stratum corneum. Between them is the transitional layer of alligators of both sexes, one pair of scent glands opens into cells transformed into the keratinized surface of the corneum the cloaca, another pair opens on the margins of the lower (figure 6.14b). Integument 221  Melanin Stratum corneum granules Transitional layer Epidermal Stratum intermedium Epidermis cell Chromatophore Stratum basale (in epidermis) Dermis Chromatophore Blood capillary (a) (b) FIGURE 6.14 Bird scales and skin. (a) Epidermal scales are present on the feet and legs of birds. (b) Section of skin showing the stratum basale and the keratinized surface layer, the stratum corneum. Cells moving out of the basal layer move through first the stratum intermedium and transitional layer before reaching the surface. These middle layers are equivalent to the spinosum and granulosum layers of mammals. (a) After Smith; (b) after Lucas and Stettenheim. Bird skin has few glands. The uropygial gland, located Feathers develop embryologically from feather folli- at the base of the tail (figure 6.15a), secretes a lipid and pro- cles, invaginations of the epidermis that dip into the under- tein product that birds collect on the sides of their beak and lying dermis. The root of the feather follicle, in association then smear on their feathers. Preening coats the feathers with with the dermal pulp cavity, begins to form the feather. this secretion, making them water repellent, and probably The old feather is shed (molt), and the beginning of a conditions the keratin of which they are composed. Follow- new feather, the feather filament (or pin or blood feather), ing a molt, preening also helps the newly regenerated feather soon grows out of the follicle as a consequence of cell prolifer- unfurl and assume its functional shape. The other gland, ation at the follicular base (figure 6.16a).The new epidermal located on the heads of some birds, is the salt gland, which is cells form three distinct tissues: a supportive but later dispos- well developed in marine birds. Salt glands excrete excess salt able sheath around the growing feather; the main feather obtained when these birds ingest marine foods and seawater. tissues themselves that later unfurl to assume their final, func- tional shape; and pulp caps that temporarily protect the Salt excretion (p. 560) delicate dermal core. As the growing spathe begins to unfurl Feathers distinguish birds from all other living verte- (figure 6.16b), new protective caps form one below the other brates. Feathers can be structurally elaborate and come in a as older pulp caps are shed together with the upper portions of variety of forms. Yet feathers are nonvascular and nonner- the sheath sloughed during preening. Further growth length- vous products of the skin, principally of the epidermis and the ens the feather as its spathe continues to deploy (figure 6.16c). keratinizing system. They are laid out along distinctive tracts, When spathe development is complete, the development of termed pterylae, on the surface of the body (figure 6.15a). the calamus begins within the same sheath at the base of the Via one or several molts, they are replaced each year. feather. The fully formed feather, embraced about its base by Generally the modern bird feather is built from a tubu- the feather follicle, is now in place (figure 6.16d). lar central shaft, the rachis, which carries on either side a vane, In a sense, a feather is a sheet of mature, dead ker- a series of barbs with interlocking connections termed atinocytes that is full of slits. This is accomplished by the barbules (hooklets). The rachis and attached vanes consti- remarkable patterning zone that determines number, shape, tute the spathe (figure 6.15b). The rachis continues proximal and spacing between cells and cell populations that form as the barbless calamus, or quill, which anchors the feather to the feather primordium. As barb ridges of the young spathe the body and often is moved by attached dermal muscles. In are delineated by the patterning zone, so are the future slits modern birds, feathers are of many types serving different func- and spaces that will appear between them. Calamus forma- tions (figure 6.15c). Flight feathers are long and the vanes asym- tion differs from that of the spathe in that no slits appear, metrical about the stiffening rachis; those flight feathers on the and a tubular calamus is produced. wings are remiges (sing, remix) and those on the tail rectrices These regeneration events are summarized in figure 6.17, (sing, rectrix). Contour feathers, or pennaceous feathers, cover which shows a highly schematic, telescoped abstract of the body and usually have symmetrical vanes about a rachis. feather development. During feather regeneration, induc- Down feathers, or plumulaceous feathers, lack a distinctive tive interaction between the dermal papilla and base of the rachis and noninterlocking barbs extend out from the calamus follicle establishes a zone of cell proliferation, where new as a fluffy feather important in insulation (figure 6.15b). keratinocytes are produced, and a zone of patterning just 222 Chapter Six kar24239_ch06_212-239.qxd 12/22/10 3:43 PM Page 223 Spathe Vane Rachis Pterylae Down Interlocking feather barbules Uropygial gland Contour Barb Ventral Dorsal feather (a) (b) Feather types Calamus Vane Barb Rachis Contour FIGURE 6.15 Feather tracts and feather feather morphology. (a) Feathers arise along specific pterylae or feather tracts. (b) General morphology of contour and down feathers. (c) Feathers types. Flight feathers constitute the major locomotor surfaces. Contour feathers on the body aerodynamically shape the surface of a bird. Down feather Filoplume Filoplumes are often specialized for display. Calamus (quill) Down feathers lie close to the skin as Flight feather thermal insulation (c) Feather types (a, c) After Smith; (b) after Spearman. above it that will generate the morphogenetic signals pre- once the differentiated feather is mature and ready to siding over the fates of these keratinocytes. In the follicle, unfurl. The spathe is the first part of the young feather to rings of outer cells (beta-keratin), the sheath and feather differentiate beneath the sheath. As the tip of the spathe itself, form more or less concentrically around the inner unfurls, the base of the spathe is still under construction. stratum cylindricum and pulp caps (alpha-keratin), and der- When the spathe completes its differentiation, the calamus mal core (figure 6.17, cross sections). The feather filament is next formed, also in the same region beneath the sheath. continues to grow out from the follicle accompanied by the As calamus formation proceeds, pulp caps continue to form highly vascularized dermal core, which extends through the within its hollow core as the dermal core regresses within follicle mouth above the surrounding integument. Core the follicle. Dermal muscles, connected in a network of tissues are protected from desiccation and trauma by a suc- muscles, act to erect mobile feathers. cession of pulp caps derived from the stratum cylindricum. The patterning process is complex. New keratinocytes The protective sheath, important initially as a scaffold formed in the proliferation zone move up in the follicle to the developing feather, is eventually lost to preening but their fates are determined in the patterning zone by Integument 223 kar24239_ch06_212-239.qxd 12/22/10 3:43 PM Page 224 Pulp caps shed Feather Sheath filament slough Skin Dermal surface core Feather follicle Dermal papilla (a) (b) (c) (d) FIGURE 6.16 Feather growth. Molting and developmental sequence of feather replacement. (a) The old feather is shed (molt), and a new feather filament soon grows out of the follicle as a result of cell proliferation at its base. (b, c) Successive stages in spathe development. Note that some tissues necessary for initial development (sheath, pulp caps) now lose this function and are sloughed off as the mature feather emerges. (d) Mature, new feather in place. Based on the research of P. F. A. Maderson and W. J. Hillenius morphogenetic signals emanating from the patterning zone. not only sets cell fates but also presides over the spacing Here cells become programmed to form sheath, pulp caps, between feather parts, and also programs cells destined to form barbs, barbules, or rachis. Cells moving through the patterning the sheath, pulp caps, and possibly the stratum cylindricum as zone receive different signals than cells that precede or follow well as the feather primordium itself. The rachis is not formed them, leading to the highly specific differentiation of the by the fusion of several barbs but also by this patterning process. emerging feather. As the spathe is being differentiated, the pat- terning process sets aside populations of keratinocytes, for Functions There are several types of feathers (figure 6.15b). example, tissues of the future barb, barbules, and rachis. Addi- Contour feathers aerodynamically shape the surface of the tionally, other signals also establish precisely patterned fates bird. Down feathers lie close to the skin as thermal insula- where cells will lose their connections to one another and form tion. Filoplumes are often specialized for display, and the future spaces and slits between barbs and barbules. Thus flight feathers constitute the major aerodynamic surfaces. the patterning zone not only sets cell fates forming structures Flight feathers of the wings are a type of contour feather. of the spathe, but also presides over the ultimate spacing They are characterized by a long rachis and prominent between feather parts. During deployment, this spacing allows vanes (figure 6.15). These feathers have some value as adjacent barbs and barbules to separate as they unfurl. Preening insulation, but their primary function is locomotion. Most of the emerging spathe encourages the overlap and interlock- feathers receive sensory stimuli and carry colors for display ing of barbules as the mature feather takes final shape. When or courtship. Chromatophores occur within the epidermis, this completes, calamus formation begins. The patterning and their pigments are carried into the feathers to give process now specifies a different outcome, namely, uninter- them color. But light refraction on the feather barbs and rupted adhesion of keratinocytes and no spaces, thereby form- barbules also creates some of the iridescent colors that ing this tubular base of the feather. Thus the patterning zone feathers display. 224 Chapter Six kar24239_ch06_212-239.qxd 12/23/10 4:27 PM Page 225 Shed pulp cap Rachis Unfurled spathe Barb Shed sheath Sheath Rachis Deployment Vane zone S.cylindricum Barb ridge Dermal core Future deployment zone (a) Pulp caps Dermal core S.cylindricum (a) Calamus Sheath Feather follicle (b) Epidermis (b) Dermis Feather follicle Patterning zone Proliferation zone Dermal papilla Dermal muscle FIGURE 6.17 Feather regeneration, summary. The highly schematic, compressed summary of feather development is shown. Cross sections of the regenerating feather are at the right to show the arrangement of concentric layers involved. At the base of the feather follicle, morphogenetic signaling between the dermal papilla and epidermal wall of the follicle establishes a proliferation zone and patterning zone.The new feather, first the spathe and later the calamus, develops between the sheath and stratum cylindricum, which together are wrapped around the dermal core.The dermal core is highly vascularized and has both supportive and nutritive functions. S. cylindricum ⫽ Stratum cylindricum. (a) and (b) Arrows indicate approximately where the cross sections are taken. Based on the research of P. F. A. Maderson and W. J. Hillenius Integument 225 Evolution of Feathers When we think of feathers, we If the protoavian limb were not streamlined, then pressure think of their roles in flight, but they likely had other func- drag would result and turbulence would have reduced aero- tions when they first arose. One view is that feathers, or dynamic efficiency. However, surface scales projecting from their scaly predecessors, played a role in surface insulation. the trailing edge of the limb would have streamlined the Surface insulation, of course, holds heat in or shields the limb, reduced drag, and thus been favored by selection. body from taking up excess heat. Either may have been the initial advantage of feathers. Surface insulation would Aerodynamic principles (p. 145; p. 361) have interfered with the absorption of environmental heat, Regardless of whether they evolved first for gliding or a disadvantage if the ancestors of birds were ectothermic. for insulation, feathers were modified from reptilian scales However, many species of ectothermic lizards have enlarged or at least from the common inductive interaction between surface scales. Once the basking lizard is warmed, it turns dermis and epidermis. In modern birds, feathers that serve so that the scales act like many tiny parasols to shade the flight are highly modified. Interlocking barbs and barbules skin surface and block further uptake of solar radiation give some structural integrity to the flexible flight feather. (figure 6.18). Once enlarged and shaped for heat exclusion, In flight feathers, the rachis is offset, making the vane asym- these protofeathers would be preadapted for heat retention or metrical (figure 6.19a). This design affects the action of the for flight. flight feather during wing beats. On the downstroke, the pres- Others argue that the ancestors of birds were sure on the underside of each feather acts along its anatomi- endothermic. In this view, protofeathers initially functioned cal midline, the center of pressure. But because the rachis is to conserve internally produced body heat. The evolution of offset, the result is to twist the feather slightly about its point aerodynamic devices serving flight came later. of attachment to the limb, forcing feathers of the wing Whether beginning with an ectotherm or an together into a broad surface that presses against the air and endotherm, many still suggest that feathers played a role in drives the bird forward (figure 6.19b). On the upstroke, the surface insulation when they first appeared and became center of pressure is now across the topside of the asymmetri- secondarily co-opted for a role in flight. However, early birds cal feather and forces it to twist in the opposite direction, and their immediate dinosaurian ancestors lacked nasal opening a channel between the feathers (figure 6.19c). This turbinates, a character diagnostic of warm-blooded physio- reduces their resistance to the airstream and allows the wing logy. If serving as insulation, these first feathers would have to recover and prepare for the next power downstroke. had a more complicated role than previously thought. Bird flight (p. 359) This controlled twisting of flight feathers passively Dinosaurs: Hot to Cold—The Sequel (p. 46); responding to wing beat depends on the asymmetrical design Turbinates (pp. 276, 495) of the feather and hence on the action of air pressure against A different view entirely stems from the argument that it during powered flight. A close look at the wing feathers of feathers evolved initially as aids to gliding and then to flight. Archaeopteryx also reveals an offset rachis and an asymmet- Feathers were selected because of their favorable effect on the rical vane (figure 6.20). This suggests that by the time of airstream passing over the body or limbs of a gliding animal. Archaeopteryx powered flight had already evolved. Mammals As in other vertebrates, the two main layers of the mam- malian skin are epidermis and dermis, which join and inter- face through the basement membrane. Beneath lies the hypodermis, or superficial fascia, composed of connective tissue and fat. Epidermis The epidermis may be locally specialized as hair, nails, or glands. Epithelial cells of the epidermis are keratinocytes and belong to the keratinizing system that forms the dead, superficial cornified layer of the skin. The surface keratinized cells are continually exfoliated and replaced by cells arising primarily from the deepest layer of FIGURE 6.18 Hypothetical scale, intermediate the epidermis, the stratum basale. Cells within the basale stage between an enlarged reptile scale and an early bird divide mitotically, producing some that remain to main- feather. Some living lizards use enlarged scales to reflect away tain the population of stem cells and others that are excess solar radiation. Subdivision of the scale provides the pushed outward. As they are displaced to higher levels, flexibility required for free movement in an active animal. they pass through keratinization stages exhibited as After Regal. distinct, successive layers toward the surface: stratum 226 Chapter Six kar24239_ch06_212-239.qxd 12/22/10 3:43 PM Page 227 Axis of rotation Axis of rotation (b) Downstroke (a) (c) Upstroke FIGURE 6.19 Flight function of asymmetrical feather vane. (a) Wing is extended, as it might appear during the middle of the power downstroke. One of the primary feathers (highlighted) is removed to show the axis of rotation about its calamus, where it attaches to the limb. (b,c) Cross sections through three flight feathers during the downstroke (b) and upstroke (c). During the power downstroke, air pressure against the underside of the wing would be experienced by each feather along its center of pressure down the anatomical midline of the feather. Because the rachis is offset, however, this center of pressure forces the feather to rotate about its axis, and the primary feathers temporarily form a closed, uniform surface. During the recovery upstroke, air pressure against the back of the wing forces rotation in the opposite direction, spaces open between feathers, and air slips between the resulting slots, thus reducing resistance to wing recovery. In addition to these epithelial cell types, the other prominent cell type that becomes secondarily associated with the epidermis is the chromatophore. Chromatophores arise from embryonic neural crest cells and may be found almost anywhere within the body. Those that reach the skin occupy sites within the deeper parts of the epidermis itself. FIGURE 6.20 Archaeopteryx feather. This feather They secrete granules of the pigment melanin, which are from the wing of Archaeopteryx shows the asymmetrical design of passed directly to epithelial cells and eventually carried into the vane, suggesting that it may have been used during powered the stratum corneum or into the shafts of hair. Skin color flight as in modern birds. results from a combination of the yellow stratum corneum, Based on Ostrom. the red underlying blood vessels, and the dark pigment gran- ules secreted by chromatophores. spinosum, stratum granulosum, often a stratum lucidum, Dermis The mammalian dermis is double layered. The and a stratum corneum (figure 6.21). The process of kera- outer papillary layer pushes fingerlike projections, termed tinization is most distinct in regions of the body where the dermal papillae, into the overlying epidermis. The deeper skin is thickest, as on the soles of the feet. Elsewhere, these reticular layer includes irregularly arranged fibrous con- layers, especially the lucidum, may be less apparent. nective tissue and anchors the dermis to the underlying fas- Keratinocytes are the most prominent cell type of cia. Blood vessels, nerves, and smooth muscle occupy the the epidermis. Other types are recognized, although their dermis but do not reach the epidermis. The mammalian functions are less clearly known. The Langerhans cells are dermis produces dermal bones, but these contribute to the stellate cells dispersed singly throughout the upper parts of skull and pectoral girdle and only rarely form dermal scales the stratum spinosum. Current evidence suggests that they in the skin. One exception is Glyptodon, a fossil mammal play a role in cell-mediated actions of the immune system. whose epidermis was underlaid by dermal bone. A similar The Merkel cells, originating from the neural crest and situation exists in the living armadillo. These species repre- associated with nearby sensory nerves, are thought to sent secondary developments of dermal bone in the mam- respond to tactile stimulation (mechanoreceptors). malian integument. Integument 227  B O X E S S AY 6. 3 “Poisonous” Birds The hooded pitohui is a brightly colored songbird, one of per- haps half a dozen related species endemic to the forests of New Guinea.This species is the first documented toxic bird. Its skin and feathers are laced with a potent neurotoxin, which if touched, causes numbness and tingling. This distributed neurotoxin is thought to provide the pitohui with some protection from ectoparasites. Apparently, the bird’s poison also works to repel snake and hawk attacks, which might also account for the bright coloration announcing its toxicity to predators. The neurotoxin itself is not manufactured by the pitohui, but is acquired from a beetle that the bird can safely eat and commandeer its toxins for the pitohui’s own defense. This same neurotoxin, formally batra- chotoxin, is also found in some poison dart frogs, likely obtained from the same or similar insect source. BOX FIGURE 1 The hooded pitohui, black headed and bright orange breast, held in a protected hand. The choresine beetle, inset and slightly enlarged proportionately, is the source of the neurotoxin that forms the bird’s chemical defense from ectoparasites and natural predators. Photos kindly supplied by and based on the research of John P. Dumbacher. Blood vessels and nerves enter the dermis. Hair follicles continuous, keratinization within the hair follicle is local- and glands project inward from the epidermis (figure 6.20). ized and intermittent. The dermis is usually composed of irregularly arranged fibrous The hair shaft grows out of the living hair follicle, connective tissue that is often impregnated with elastic fibers which goes through a cycle of activity with three stages— to give it some stretch but return it to its original shape. As a growth, degeneration, rest. During growth, there is active person ages, this elasticity is lost, and the skin sags. proliferation of cells in the hair papilla at the base of the hair, producing successive addition to the hair shaft, which Hair Hairs are slender, keratinous filaments. The base of emerges from and continues to lengthen from the skin sur- a hair is the root. Its remaining length constitutes the non face. At the end of the growth stage, the hair-producing cells living shaft. The outer surface of the shaft often forms a scaly become inactive and die, entering the degeneration stage. cuticle. Beneath this is the hair cortex, and at its core is the Thereafter the follicle enters the resting stage, which may hair medulla (figure 6.21). last for several weeks or months. Eventually, stem cells in the The hair shaft projects above the surface of the skin, papilla produce a new follicle and the growth stage begins but it is produced within an epidermal hair follicle rooted again. At about this time the old hair shaft falls out to be in the dermis. The surface of the epidermis dips down into replaced by the new growing shaft. The cycle is intrinsic and the dermis to form the hair follicle. At its expanded base, cutting the hair seems not to accelerate hair growth. the follicle receives a small tuft of the dermis, the hair Chromatophores in the follicle contribute pigment papilla. This papilla seems to be involved in stimulating granules to the hair shaft to give it further color. The arrec- activity of the matrix cells of the epidermis, but does not tor pili muscle, a thin band of smooth muscle anchored in the itself directly contribute to the hair shaft. The tiny clump dermis, is attached to the follicle and makes the hair stand of living matrix cells, like the rest of the stratum basale, is erect in response to cold, fear, or anger. As humans (and the germinal region that starts the process of keratiniza- many other mammals) age their hair becomes gray, no mat- tion to produce hair within the follicle. Unlike kera- ter what their original youthful color. This occurs because tinization within the epidermis, which is general and special stem cells responsible for hair color within the hair 228 Chapter Six  Cuticle Cortex Medulla Melanin S. corneum FIGURE 6.21 S. lucidum Mammalian skin. The epidermis Epidermis S. granulosum is differentiated into distinct layers. S. spinosum As in other vertebrates, the S. basale deepest is the stratum basale, which through mitotic division produces cells that as they age become succ