Linzey: Vertebrate Biology 8. Reptiles: Morphology, Reproduction, and Development Text © The McGraw−Hill Companies, 2003 CHAPTER 8 Reptiles: Morphology, Reproduction, and Development (a) Bones of carapace (b) Bones of plastron (c) Scales of carapace (d) Scales of plastron Entoplastron Epiplastron Hypoplastron Mesoplastron Hypoplastron Xiphiplastron Intergular Gular Humeral Pectoral Abdominal Femoral Anal Axillary Intramarginal Inguinal Peripheral Neural Nuchal Costal p p p p p p p p m m m m m m m m m m m p p p v Vertebral Pleural Cervical Marginal Supramarginal v v v p PeripheralSuprapygal Pygal n n n n n n n s s s s s s s s c c c c c c c Upper: Dermal bones forming the carapace (a) and plastron (b) of a turtle. Lower: Epidermal scales covering the carapace (c) and plastron (d) of a turtle. FIGURE 8.1 ■ INTRODUCTION Reptiles, comprising over 16,150 of the 53,000; species of vertebrates, include turtles (230 species), tuataras (2 species), lizards (3,900 species), snakes (2,400 species), crocodilians (21 species), and birds (9,600 species). With the evolution of internal fertilization and the amniote egg, reptiles became the first fully terrestrial vertebrates. T URTLES ,T UATARAS ,L IZARDS , AND S NAKES (T ESTUDOMORPHA AND L EPIDOSAUROMORPHA ) ■ MORPHOLOGY Integumentary System Turtles and lepidosaurs possess scales that, unlike those of fishes, are formed mainly from epidermal layers. The dry, scaly epidermis, which may be six or more layers in thickness, serves primarily for protection and to reduce water loss. Some snakes utilize the broad, flat scales, known as scutes, on the undersides of their bellies to aid in locomotion. In turtles, the shell of dermal plates (Fig. 8.1a, b) is covered by horny, ker- atinized scales (also known as shields or scutes) (Fig. 8.1c, d). The embryonic origin and morphology of the integument in reptiles is discussed by Maderson (1985). In squamates (snakes and lizards), the epidermis consists of a stratum corneum (outer tissue layer) and a stratum inter- medium (middle tissue layer) above the stratum basale (basal cell layer) (Fig. 8.2a, b). In most lizards and snakes a contin- ual body covering of scales develops from the stratum corneum, with each scale projecting backward to overlap part of the one behind. In turtles, however, each epidermal scale develops sep- arately, so that the scales do not form a solid sheet. The num- ber and arrangement of epidermal scales on the body is usually species-specific and is used extensively in classification. The stratum corneum is sloughed and replaced either a few cells at a time or in patches, or it is shed at intervals in Linzey: Vertebrate Biology 8. Reptiles: Morphology, Reproduction, and Development Text © The McGraw−Hill Companies, 2003 Reptiles: Morphology, Reproduction, and Development 199 (a) Resting stage Stratum corneum Stratum germinativum Basement membrane Slough (b) Before sloughing (d) Sloughing (c) Shortly before sloughing B A og og k ig oa New og ig cz Old ig Next og FIGURE 8.2 Simplified diagrams showing changes in the epidermis during the sloughing cycle of a snake. (a) Resting stage. (b) Before sloughing. The basal cells have divided to form a new, inner epidermal generation (ig). The snake’s color is dulled. (c) Shortly before sloughing. A cleavage zone appears between the two generations; the superficial part of the inner generation is becoming keratinized (k), and a new serrated outer epidermal generation (og) is being formed. This stage probably coin- cides with the clearing of the skin. (d) Sloughing. The original outer generation is shed, and the old inner generation becomes the next outer generation. one piece, a process known as ecdysis. Healthy snakes usu- ally shed their skins in one piece, whereas most lizards nor- mally shed their skin in a number of pieces (Fig. 8.3). Old scales on some turtles peel off; in other species of turtles, the scales remain and give the shell a roughened texture. When ecdysis begins, the two epidermal layers separate simultaneously over the entire body, and the outer layer is removed (Fig. 8.2). The stratum corneum is loosened pri- marily through the diffusion of lymph and white blood cells between the old and new layers. Shortly before shedding begins, the separation of the scales covering the eyes of snakes causes the eyes to become cloudy. As the outer layer of epi- dermis is removed, the inner layer becomes the new outer layer. Ecdysis normally begins in the head region and is ini- tiated by an increase in blood pressure that causes the head to enlarge. This swelling causes the outermost layer of cells to loosen and rupture. Then, by means of the animal’s rub- bing and crawling movements, the remainder of the outer layer is removed. After a week or so, the stratum germina- tivum will have produced enough new cells through mitosis to form a new inner tissue layer. Frequency of shedding varies with species, age, and the health of the animal. Few integumentary glands are present in reptiles. Those that are present (musk, femoral, pre-anal, cloacal, and nuchodorsal) either secrete strong-smelling substances that may be obnoxious to potential predators or serve for species and sex recognition (pheromones) during breeding. No sweat glands are present. Scales, claws, rattles, horny protuberances, and spines are all keratinized modifications of the epidermis. Claws, which first appeared in turtles and have persisted in birds and most mammals, are shed periodically in turtles and lepidosaurs; however, in birds and mammals, claws, nails, and hooves are worn down by abrasion. Many lizards can climb vertical surfaces readily by using their sharp claws. Some climbing lizards, such as geckos and anoles, utilize “dry” adhesion systems on their toes as addi- tional aids when climbing on steep smooth surfaces and over- hangs (Cartmill, 1985) (Fig. 8.4a, b). On the underside of each toe are approximately 20 broad overlapping scales (lamellae) consisting of numerous minute setae composed of keratin (Ruibal and Ernst, 1965; Ernst and Ruibal, 1966). Up to 150,000 hairlike setae are located on the exposed sur- face of each lamella. The setae are so small that their inter- molecular interactions with the surface enable the gecko to adhere to the surface. A gecko’s ability to walk on a vertical surface is directly correlated with that surface’s molecular polarity and not with the degree of microscopic abrasions on that surface (Hiller, 1975). The many close contacts assure that the animal adheres as if it had climbing shoes with thou- sands of minute cleats imbedded in the substrate. Rattlesnake rattles are modified portions of the stra- tum corneum that remain attached to the tip of the tail fol- lowing each ecdysis (Fig. 8.4c). The rattles interlock in such a way that they fit together more tightly dorsally than ven- trally. The rapid oscillation of the tail and its horny appendage produces the characteristic buzzing sound of an agitated rattlesnake. Because lobes of the rattle often are bro- ken off accidentally, and because snakes may shed their skins several times a year, the age of a rattlesnake cannot be deter- mined accurately by simply counting the number of seg- ments in the rattle. The horns of the horned “toad” (a lizard) (Phrynosoma sp.) are bony projections of the occipital bone of the skull cov- ered with scaly integument, whereas the hornlike processes on the head of the sidewinder rattlesnake (Crotalus cerastes) are exclusively integumental in origin. A horny sheath of FIGURE 8.3 Ecdysis in a lizard. Most lizards shed their skin in pieces, whereas healthy snakes usually shed their skins in one piece. Linzey: Vertebrate Biology 8. Reptiles: Morphology, Reproduction, and Development Text © The McGraw−Hill Companies, 2003 200 Chapter Eight Electronic Publishin g Services Inc. (b) Setae borne by the lamella Bristles and endplates borne by the setae (a) Toe with imbricated lamellae (c) Modifications of the stratum corneum of lizards and snakes. (a) The toe pads of climbing lizards such as geckos employ “dry” adhesion systems as addi- tional aids when climbing on steep smooth surfaces and overhangs. (b) The lamellae of the toes are composed of many setae, whose distal ends bear bristles and endplates. (c) One modification of the stratum corneum in reptiles is the rattlesnake’s rattle, which consists of pieces of thickened skin left behind each time the snake sheds. FIGURE 8.4 lateral bridges. Nuchal and costal plates of the carapace are fused with vertebrae, and each costal plate is united with a rib. Soft-shelled and leatherback sea turtles have leathery shells, because the dense collagenous connective tissue of the dermis does not become ossified. A few lizards, such as skinks and glass lizards, have similar, but smaller, bony dermal scales (osteoderms) that serve to reinforce their scales. The dermis has an abundance of chromatophores, which are responsible for elaborate color patterns. Although several speculative mechanisms for pigment pattern forma- tion have been proposed, the actual mechanism of color pat- tern formation is not known. Some lizards, such as stratum corneum covered the beaks of some extinct reptiles and continues to cover the beaks of living turtles. The dermis consists of a relatively loosely packed super- ficial layer and a much more densely packed deeper layer. As in other vertebrates, it consists of fat cells, nerve fibers, blood vessels, and chromatophores. The skin of cotylosaurs (stem reptiles) was heavily armored with large bony dermal scales. Today, turtles are the most armored members of this group, with a shell con- sisting of large, bony, dermal plates (Fig. 8.1a, b). The dor- sal arched portion of the shell is the carapace; the ventral, flattened portion is the plastron. These are united by bony Linzey: Vertebrate Biology 8. Reptiles: Morphology, Reproduction, and Development Text © The McGraw−Hill Companies, 2003 Reptiles: Morphology, Reproduction, and Development 201 FIGURE 8.5 The snake skeleton in this x-ray image has more than 300 vertebrae and 400 ribs. A large number of vertebrae gives the snake flexibility and allows it to bend and twist more than most vertebrates. chameleons, change their color in response to environmen- tal stimuli by concentrating and dispersing pigment gran- ules. Coloration may be protective (camouflage and warning patterns), may reflect dominant social status, may serve for sex recognition, or may be important in thermoregulation. Color patterns of many snakes involve spots or stripes. Spotted patterns are usually thought to serve as camouflage and are most common in species that feign immobility when approached. Stripes, which make it hard to judge the speed of a moving object, are characteristic of species that flee when threatened. Brodie (1989) demonstrated a genetic link between behavior and pattern in newborn garter snakes (Thamnophis ordinoides) in which striped individuals tended to flee, whereas spotted individuals tended to remain motionless. Skeletal System Skeletal modifications for terrestrial life that originated in amphibians are developed further in reptiles. The skeleton shows numerous modifications for muscle attachment, var- ied dietary habits, and terrestrial locomotion. Reptiles can better support their body weight and, in many cases, can move with great speed. Papers discussing various aspects of the skeleton are included in Gans et al. (1969). Adult reptilian skulls differ from those of amphibians in many ways (see Fig. 6.13). A single occipital condyle is pre- sent, the skull has a higher and narrower shape, a greater degree of ossification is present, and a reduction of bones through loss and/or fusion has occurred. A partial secondary palate is present in many turtles. Quadrate and articular bones form in the skull from gill arch supports. The hyomandibular becomes the columella (stapes) in the middle ear, and the roof of the skull, palate, and lower jaw become ensheathed in dermal bones. The sym- physis of the anterior ends of the two dentaries, the major tooth-bearing bones in the lower jaw, is a rigid suture in some turtles and some lizards, but in snakes and many lizards it is connected by ligaments. Independent movement of the upper jaw on the braincase is well developed in some snakes and allows for great distensibility of the mouth, an adaptation necessary for swallowing large prey. Some palatine bones as well as the jaws are connected so loosely to the skull that each half of the upper and lower jaws can move independently of each other (see discussion in Digestive System, page 208). Amphibians and many reptiles swallow their food whole; thus, having internal nares in the anterior portion of the oral cavity presents no problem. Others (especially nonmam- malian synapsids) tore, crushed, and chewed their food before swallowing. To avoid interrupting their breathing, it became necessary to get air into the pharynx posterior to the chewing mechanism. Turtles developed a secondary palate below the primary palate. The secondary palate, which separates the nasal pas- sages from the oral cavity, serves to increase the length of the nasal passages and permits an animal to breathe while pro- cessing food in its mouth. This latter adaptation (ability to breathe and chew food simultaneously) is seen as a link to the development of higher metabolic rates leading to the origin of endothermy in Therapsida. Lepidosaurians (lizards, tuataras, and snakes) lack a secondary palate. A feature seen for the first time in the evolution of ver- tebrates is the development of either one or two pairs of fen- estrae (fossae) in the temporal region of the skull (see Figs. 7.2 and 7.5). These fenestrae provide additional surface area for stout muscles that originate from the temporal region of the skull and insert on the lower jaw, enabling it to close with increased pressure. Temporal fenestrae are major char- acters used in reptilian classification systems. Stem reptiles (order Cotylosauria) lacked fossae, a con- dition referred to as anapsid. Today, the only living reptiles with anapsid skulls are turtles (order Chelonia). Extinct mammal-like reptiles (order Therapsida) developed a single pair of temporal fossae low on each side of the skull. This synapsid type of skull is found in extant mammals. Diapsid skulls have two pairs of fossae (superior and inferior) on each side of the skull. Diapsid skulls are characteristic of extinct archosaurs, surviving archosaurs (crocodilians), and the tuatara (Sphenodon). Lizards, snakes, and birds have modi- fied diapsid skulls. The reptilian vertebral column has undergone additional modifications and exhibits a wide range of types and arrange- ments of vertebrae. Snakes have the longest vertebral columns, with up to 500 vertebrae (Fig. 8.5). Most turtles and lepidosaurs have a variable number of cervical vertebrae. In addition, for the first time in the evolution of vertebrates, the first two cervical vertebrae have become modified to per- mit movements of the head in several directions. The first vertebra (atlas) is ringlike because most of its centrum has been detached. It articulates with the single occipital condyle on the skull. The second cervical vertebra (axis) has an ante- rior projection, known as the dens or odontoid process, that rests on the floor of the atlas when the two vertebrae are Linzey: Vertebrate Biology 8. Reptiles: Morphology, Reproduction, and Development Text © The McGraw−Hill Companies, 2003 202 Chapter Eight (a) Salamander (b) Placental mammal Cleithrum Scapula Humerus Coracoid Interclavicle Scapula Humerus Clavicle FIGURE 8.6 Evolution of limb structure. (a) Salamander. The sprawled posture of the salamander was typical of fossil amphibians as well as of most reptiles. (b) Placental mammal. This posture began to change in synapsids, so that in late therapsid reptiles the limbs were thought to be carried more beneath the body, resulting in better support and more rapid locomo- tion. As a result of the change in limb posture, the shoulder girdle also became modified. A sprawled posture brings a medially directed force toward the shoulder girdle, with medial elements playing a major role in resisting these forces. As limbs were brought under the body, these forces were directed less toward the midline and more in a vertical direction. This position of the limbs might account for the loss of some elements of the pectoral girdle in those phylogenetic lines in which the limb posture shifted. articulated. It represents the detached centrum of the atlas. Cervical vertebrae of turtles are loosely articulated in order to allow the neck to be pulled back into the shell. In most lizards, trunk vertebrae have differentiated into thoracic vertebrae that bear ribs, and lumbar vertebrae with ribs greatly reduced or absent. The vertebral column of snakes and legless lizards is divided into two regions: a precaudal (anterior to the vent) series of vertebrae, which bear free ribs; and a postcaudal (posterior to the vent) series with ribs either fused to the vertebrae or absent altogether. Zygapophyses (processes by which adjacent vertebrae articulate to one another) strengthen intervertebral joints. Most living reptiles possess two sacral vertebrae, which usually are fused to form a single bony complex, the sacrum, to support the pelvic gir- dle. The stronger sacrum provides the support necessary for raising the body off the ground as reptiles walk; some lizards and dinosaurs even adopted a bipedal mode of locomotion. All reptiles have a distinct tail composed of many cau- dal vertebrae. A unique characteristic possessed by many lizards and a few snakes is the ability to break off their tails in order to avoid capture, known as caudal autotomy. This ability is possible because the centrum and part of the neural arch of each caudal vertebra are divided in half by an area of soft tissue. The plane of fracture occurs at this point, and most of the lost portion of the tail will regenerate. Caudal autotomy as a defense mechanism has been discussed by Dial and Fitzpatrick (1983) and Arnold (1988). All vertebrae from cervicals to caudals may have ribs. The ribs of turtles, as well as the neural arches of the dorsal, sacral, and first caudal vertebrae, are fused with the carapace. Posterior cervical and anterior dorsal ribs of tuataras each bear a curved cartilaginous uncinate process, which projects posteriorly to overlap the rib behind, presumably giving strength to the thoracic body wall. In “flying dragons” (fam- ily Agamidae), five to seven posterior trunk ribs are greatly elongated to support large, thin membranes, which allow these lizards to glide distances up to 60 m. A mostly carti- laginous sternum is present in some lizards, although it is absent in snakes, legless lizards, and turtles. When present, the sternum consists of a plate to which thoracic ribs attach. The limb structure shows considerable variation related to the burrowing, terrestrial, arboreal, or aquatic habits of these reptiles. Methods of locomotion include lateral undu- lation on both land and in water (swimming), bipedal and quadrupedal gaits, and flight. Most snakes and some lizards lack an appendicular skele- ton. Clavicles are reduced or absent from the pectoral girdle in legless lizards, and the entire pectoral girdle is missing in snakes. In turtles, the clavicles are fused with the carapace. Limbs are typically pentadactyl, with five digits normally present on both the front and rear feet. Elements of the ante- rior limb are similar to those in salamanders (Fig. 8.6a). In most reptiles, a rotation of the appendages toward the body causes the long axis of the humerus and femur to lie more nearly parallel the body. A moderate bend at the elbow and knee allows the front and hindlimbs to be directed some- what vertically, and the elbow is directed caudad (toward the tail). Limbs oriented in this fashion can better support the weight of the body and serve as more efficient shock absorbers. In addition, by having the body moderately ele- vated above the ground, greater speed and agility is possi- ble. Such reorientation was an essential step toward bipedalism in reptiles. Even with this reorientation, the position of the limbs among modern quadrupedal reptiles remains a sprawling one. Complete and more efficient ele- vation comes from the limb–girdle arrangement found in birds and mammals (Fig. 8.6b). Modification of the front limb occurred in aquatic reptiles such as ichthyosaurs, plesiosaurs, and sea turtles (Fig. 8.7). The short, stout appendages tend to become flattened and paddle-shaped, and in some, the number of phalanges is greatly increased. Aquatic and semiaquatic reptiles often have webbing between the toes. Linzey: Vertebrate Biology 8. Reptiles: Morphology, Reproduction, and Development Text © The McGraw−Hill Companies, 2003 Reptiles: Morphology, Reproduction, and Development 203 Humerus Pisiform Ulna Radius (a) Ichthyosaur Flat pisiform widens wrist Phalanges long Carpals Metacarpals (b) Sea turtle FIGURE 8.7 Front limb of (a) an ichthyosaur and (b) a sea turtle (Chelonia). The limbs are short, stout, and often have an increased number of phalanges. FIGURE 8.8 (a) The pelvic region of a boa constrictor, showing its vestigial pelvic girdle; pg, vestigial pelvic girdle. (b) The presence of a vestigial pelvic limb in boas, pythons, and a few other groups is associated with small claws or spurs located on either side of the vent. Male boas and pythons use their spurs, which are often longer than those of females, to stimulate females during courtship. Each half of the pelvic girdle consists of a pubis, ischium, and ilium. The ilium is braced against two sacral vertebrae and tends to become broader for the attachment of larger hindlimb muscles, particularly in dinosaurs and lizards that carry the trunk elevated well above the ground. In reptiles that have lost the hindlimbs, the pelvic girdle has been reduced (legless lizards) or lost (most snakes). Bony elements in the posterior limbs are similar to those in amphibians. The knee is directed anteriorly, and the ankle joint is located between two rows of tarsal bones rather than between the tarsals and the tibia and fibula. A patella, or kneecap, is present for the first time and occurs in certain lizards. The order Squamata (lizards and snakes) is the only group of vertebrates in which there has been evolutionary losses of limbs and redevelopment of undulatory body move- ments. Snakes are thought to have evolved from lizards and to have lost both pairs of limbs as well as both girdles. Some primitive families such as the Boidae, however, still possess vestigial pelvic girdles and/or rear legs (Fig. 8.8a, b). Differ- ent stages of reduction and loss of limbs are found in lizards. Some possess only vestiges of forelimbs, some have only hind- limbs, and others, such as glass lizards (Anguidae), have lost all of their limbs. Most species that lack limbs (snakes, legless lizards) move by horizontal undulations (Fig. 8.9a). This method, in which all parts of the body move along the same wavy track, is efficient on the ground as well as in trees. Its effec- tiveness is diminished, however, when the substrate lacks fixed surfaces or when the fixed surfaces are too widely spaced. Under these latter conditions, most snakes use con- certina-like movements in which the stationary portion of the body is bent into a series of S-shaped coils from which the moving anterior portion straightens and then bends again (Fig. 8.9b). The posterior coils press downward and backward against the substrate, relying on friction to prevent slipping. This method is used extensively by climbing and burrowing species such as boids and rat snakes (Elaphe). During rectilinear locomotion, the skin is drawn for- ward, the belly scales (scutes) make contact with the surface and provide stationary points, and then the body is pulled forward by the scutes (Fig. 8.9c). Muscles that slant backward and downward from the ribs to the scutes cause the ventral skin, which fits loosely and is very distensible, to bunch at sev- eral regions so that the scutes overlap. Between these regions, the skin is stretched. Where scutes are bunched, they rest on the ground to support the animal’s weight; where stretched, they are lifted off the ground. One by one, additional scutes are drawn into each bunched region from behind as others are stretched away anteriorly. Friction of the bunched scutes against the substrate prevents slipping. Muscles that slant backward and upward from the scutes to the ribs pull the body along within the skin. The body is held in a straight line and moves directly ahead. Rectilinear movement is slow and may be used by snakes and worm lizards (amphisbaenians) when stalking prey or moving in narrow tunnels. Sidewinding is unique to snakes, especially desert species (Fig. 8.9d). It provides for rapid travel over a smooth, (a) (b) pg Linzey: Vertebrate Biology 8. Reptiles: Morphology, Reproduction, and Development Text © The McGraw−Hill Companies, 2003 204 Chapter Eight (a) Lateral undulation (b) Concertina motion (c) Rectilinear motion (d) Sidewinding Direction of travel Move Contract Fix Stretch Move 0 sec 1 sec 2 sec FIGURE 8.9 Snake locomotion: (a) lateral undulation; (b) concertina locomotion; (c) rectilinear locomotion; (d) sidewinding. Refer to the text for a discussion of each type. unstable, and often hot substrate. The snake makes a series of tracks that are more or less straight lines, parallel to one another and angled to the direction of travel. Movement begins by the snake swinging its head, neck, and anterior body through an angle of 90° to 120° and placing its head on the ground in a new position. The remainder of the body then is lifted rapidly, section by section, from the old line of rest to the new position. The snake’s body is in contact with two or three tracks at any given time, which are constantly changing position. Parts of its body are within the tracks; other parts are arching between tracks and are held above the substrate. As each new track is made by anterior portions of the body, posterior segments are released from the previous track. The head normally starts swinging to a third track ahead of the snake’s position before the tail comes to rest on the second. The body moves forward at an angle of about 60° to the direc- tion of travel. Some snakes, such as the African desert viper (Bitis caudalis), have modified the basic sidewinding locomo- tion and are able to jump short distances in order to reduce their contact with the intense heat of the desert floor. Muscular System The muscular system of reptiles has become more differen- tiated and better adapted to terrestrial life than that of amphibians. Muscles have become modified, not only to support the viscera and the weight of the body, but also to allow for various methods of locomotion. In addition, res- piratory muscles have further differentiated and become bet- ter developed. Epaxial muscles show less modification than hypaxial muscles, with some epaxial muscles losing their metamerism and differentiating into bundles. Besides their function of allowing side-to-side movement of the vertebral column, epaxial muscles take on new functions including support and Linzey: Vertebrate Biology 8. Reptiles: Morphology, Reproduction, and Development Text © The McGraw−Hill Companies, 2003 Reptiles: Morphology, Reproduction, and Development 205 Right systemic trunk Pulmonary trunk Left systemic trunk Right atrium Left atrium Cavum venosum Cavum arteriosum Right systemic trunk Left systemic trunk Pulmonary trunk Right atrium Left atrium Cavum arteriosum Right atrium Left atrium Right ventricle Left ventricle Right ventricle Left ventricle Cavum venosum Right ventricle Left ventricle Right systemic trunk Left systemic trunk (a) Squamata (b) Chelonia (c) Crocodilia Interventricular septum FIGURE 8.10 Diagrammatic representation of cardiac circulation in two lepidosaurs (a, b) and an archosaur (c). Note the complete separation of the ventri- cles in crocodilians. From Feduccia and McGrady, Torrey’s Morphegenesis of the Vertebrates. Copyright © 1991 John Wiley & Sons, Inc. Reprinted by permission of John Wiley & Sons, Inc. vertical bending, or arching, of the back. In turtles, epaxial muscles of the rigid trunk region are poorly developed, but those of the neck and tail are well developed. The presence of ribs on most trunk vertebrae causes increased modification of the hypaxial muscles. Ribs form in the myosepta of the body wall muscles along most of the length of the vertebral column in snakes and legless lizards. The dissections of Mosauer (1935) and Gasc (1967) indicate the presence of as many as 20 discrete muscles on each side of a single snake vertebra. These muscles connect vertebra to vertebra, vertebra to rib, rib to rib, and both rib and vertebra to skin, as well as attach to longitudinal tendons that help form and control the curvatures of the body. In other rep- tiles, myosepta and ribs have become confined to the ante- rior portion of the trunk, now known as the thorax. Abdominal wall muscles lack segmentation, and they have differentiated into three layers: external oblique, internal oblique, and transversus abdominis. Hypaxial muscles of the thoracic body wall, known as intercostal muscles, assist in respiration by raising and lowering the rib cage. The body of reptiles is suspended from the scapulae by muscles that show much more differentiation than those of amphibians. Muscles of the limbs and girdles consist of dor- sal extensor and ventral flexor muscles. Increased specializa- tion of the intrinsic muscles allows for more precise and powerful movement of the limbs as well as greater support for the body. In those forms utilizing quadrupedal locomo- tion, muscles attached to the humerus and femur must rotate these bones forward and backward, as well as hold the bones steady in a horizontal position at the appropriate angle to the horizontal so that the body can be held above the substrate. Muscles of the first pharyngeal arch continue to oper- ate the jaws, and muscles of the second arch are attached to the hyoid skeleton. Muscles of the remaining arches con- tinue to be associated primarily with the pharynx and larynx. Extrinsic integumentary muscles insert on the under- side of the dermis and allow independent movement of the skin. This is the first group of vertebrates to have integu- mentary muscles capable of moving the skin. Cardiovascular System Because reptiles are the first truly terrestrial vertebrates, many differences between the reptilian and amphibian cardiovas- cular systems are associated with the loss of functional gills and the need for efficient pulmonary circulation to bring blood to and from the lungs. Reptiles exhibit three different modes of circulation (Fig. 8.10). The ventricle of reptiles other than crocodilians is incompletely divided into dorsal and ventral chambers by a horizontal septum. A smaller ver- tical septum divides the ventricles into right and left cham- bers. The pulmonary trunk leaves the right ventricle. Both systemic trunks exit from the left ventricle in the Squamata (snakes and lizards); in turtles, however, one systemic trunk leaves the left ventricle and the other leaves the right ventri- cle. Because the interventricular septum is not complete, and because both atria open into the left ventricle, blood can flow from the left ventricle into the right ventricle. The atrioventricular valve consists of two flaps that par- tially subdivide the left ventricle into a cavum arteriosum on the left and a cavum venosum on the right. When the atria contract, the cavum venosum becomes filled with deoxy- genated blood from the right atrium and the cavum arterio- sum becomes filled with oxygenated blood from the left atrium. Most of the deoxygenated blood in the cavum veno- sum flows into the right atrium. When the right ventricle contracts, the blood flows out through the pulmonary trunk, and in turtles through the right systemic trunk also. The oxy- genated blood, together with some deoxygenated blood, is pumped out from the cavum arteriosum through the left sys- temic trunk (turtles) or both systemic trunks (Squamata). Linzey: Vertebrate Biology 8. Reptiles: Morphology, Reproduction, and Development Text © The McGraw−Hill Companies, 2003 206 Chapter Eight (a) Turtle Carapace Lung Pectoral girdle Trachea PlastronHeart Liver (b) Lizard Pectoral girdle Trachea Lung FIGURE 8.12 (a) Gas exchange in the turtle. Sagittal view showing the location of the lung and its relationship to other internal organs. Since turtle lungs are enclosed by a rigid, protective shell, the fixed rib cage cannot ventilate the lungs. To compensate, turtles have sheets of muscles within the shell that contract and relax to force air in and out of the lungs. Turtles can also alter the air pressure within their lungs by moving their limbs in and out of the shell. (b) Gas exchange in a lizard. The lungs, which are located in the thoracic cavity, are surrounded by ribs and are connected to the trachea. Compression and expansion of the rib cage forces air in and out of the lungs. The internal lining of the lungs shows numerous faveoli, which give the lining a honeycomb appearance. The faveoli increase the respiratory surface area of the lung and function in gas exchange along with the capillaries that line their walls. Aortic arches III, IV, and the ventral part of VI remain in most adult turtles, lizards, and snakes, but their connections have been modified considerably (Fig. 8.11). The primitive ven- tral aorta splits into three channels: a pulmonary trunk and two aortic trunks. The pulmonary trunk leaves the right ventricle and carries blood to the lungs. One aortic trunk emerges from the left side of the ventricle and leads to the third aortic arch and to the fourth aortic arch on the right side of the body. A second aortic trunk emerges from the right side of the ventricle and leads to the fourth aortic arch on the left side of the body. Because only one lung is functional in most snakes and legless lizards, the embryonic sixth aortic arch on the lungless side is lost. The third aortic arch on that side also disappears in most snakes. Most adult snakes, therefore, possess only a right pulmonary artery and a right common carotid artery. The venous system shows little change from that of amphibians, although some modifications have occurred due to changes in the heart and kidneys and due to the elimina- tion of cutaneous respiration. Due to the latter modification, reptiles have larger pulmonary veins and smaller cutaneous veins than amphibians. Reptilian erythrocytes are oval and nucleated. They are smaller and more numerous than those of amphibians, rang- ing in length from about 15 to 23 µm. Leucocytes and thrombocytes make up the remaining cellular components of reptilian blood. Respiratory System With the formation of a secondary palate in some reptiles, the anterior part of the respiratory tract begins to be sepa- rated from the anterior part of the digestive tract. The inter- nal nares in these forms are located farther caudad and nearer the midline than in amphibians, and nasal passages are lengthened. To keep the air passageway open while large prey is being slowly swallowed, snakes have a glottis that can be protruded. In most reptiles, the trachea is about as long as the neck; it is shortest in lizards. In some turtles, however, it is longer than the neck and convoluted. Although most reptiles are voiceless, some lizards and turtles possess vocal cords, but they produce few sounds dis- cernible to the human ear. A few turtles make grunting noises, geckos “bark,” and many species of anoles emit dis- tinctive squeaks, especially when being captured. The lungs of most reptiles are located in the pleu- roperitoneal cavity and are, in most cases, better developed than amphibian lungs. In turtles and most lizards, the lungs consist of numerous large chambers, each composed of many individual subchambers, called faveoli (Fig. 8.12a, b). Inter- nal partitioning is best developed in legless lizards, with pockets of trapped air causing the lungs to be spongy. Lungs of snakes are elongate and may be paired or unpaired. In (a) Right aortic arch Left aortic arch Anuran Common carotid (b) Aortic trunk Right Left Pulmonary trunk Reptile (c) Aortic trunk Right systemic arch Bird Pulmonary trunk (d) Left systemic Pulmonary trunk Mammal Aortic trunk Ventricle Aortic trunk Pulmonary artery Common carotid Left ventricle Right ventricle Subclavian Subclavian Subclavian Subclavian Common carotid Common carotid Left ventricle Right ventricle arch Right ventricle Left ventricle FIGURE 8.11 Fate of the systemic arches in tetrapods. The systemic arches of both sides persist in adult anurans (a) and reptiles (b). Only the right systemic arch persists in birds (c), whereas only the left remains in mammals (d). Linzey: Vertebrate Biology 8. Reptiles: Morphology, Reproduction, and Development Text © The McGraw−Hill Companies, 2003 Reptiles: Morphology, Reproduction, and Development 207 tuataras (Sphenodon), the lungs continue to exist as simple sacs similar to those in amphibians. Reptiles may use a force-pump system similar to that of amphibians in order to get air into their lungs, or they may inspire air by active suction and expire by pressure. Most rep- tiles respire by expanding and compressing the pleuroperi- toneal cavity through backward and forward movements of the ribs produced through contraction of intercostal muscles. In a few snakes and lizards, the lungs are in separate pleural cavities. A tendinous transverse partition, the oblique septum, separates the pleural cavities from the coelom. Contraction of muscles tightens the septum, which lowers pressure within the lungs below that of the external atmos- phere. Because turtles are encased in a rigid shell and the ribs are fused to the carapace, the ribs cannot function in gas exchange. Instead, specialized sheets of muscle contract and relax to move air in and out of the lungs (Gans and Hughes, 1967). Reptiles depend almost entirely on lungs to aerate their blood. Some reptiles supplement gas exchange by utilizing gas exchange membranes in other areas of the body, includ- ing the pharynx (pharyngeal gas exchange), cloaca (cloacal gas exchange), and skin (cutaneous gas exchange). Pharyngeal (buccopharyngeal) gas exchange is partic- ularly well developed in soft-shelled turtles (Trionychidae) (Girgis, 1961; Dunson and Weymouth, 1965). It permits them to obtain dissolved oxygen from water and, hence, to stay underwater for long periods. Pharyngeal gas exchange also is known to occur in the Australian skink (Drummond, 1946). Cloacal gas exchange may occur in many turtles in the families Chelydridae, Testudinidae, and Pelomedusidae. The accessory cloacal bladders have been proposed as aux- iliary gas exchange structures, as water is pumped in and out of the vent when the turtles are submerged (Zug, 1993). Oxygen supposedly diffuses through the smooth and lightly vascularized walls of the bladders, and carbon diox- ide passes out. Cutaneous gas exchange has been reported in several turtles, including the soft-shelled turtle (Apalone sp.), musk turtles (Sternotherus odoratus and S. minor), mud turtles (Kinosternon subrubrum), snapping turtles (Chelydra ser- pentina), and pond sliders (Trachemys scripta) (Stone et al., 1992). Girgis (1961) reported that soft-shelled turtles obtain up to 70 percent of their oxygen by diffusion through the leathery skin covering their carapace and plastron. Shallow-diving sea turtles are thought to make aerobic dives relying on the lungs’ oxygen store. The leatherback is the largest sea turtle and the deepest diver, able to dive beyond 1,000 m (Eckert et al., 1986). Increased hydrostatic pressure probably collapses their lungs during deeper dives (Berkson, 1967), so that they may have to rely on blood and tissue stores of oxygen. The oxygen-carrying capacity of their blood is twice that of shallow-diving sea turtles (Lutcavage, 1990). Their blood volume is slightly higher, but their lung volume is considerably smaller than in other sea turtles (Lut- cavage et al., 1992). Although one lung is rudimentary or absent in legless lizards and most snakes, both lungs are functional in prim- itive snakes such as boas and pythons (family Boidae), where the left lung is about 30 to 80 percent as large as the right lung. In some snakes, such as cobras, hognose snakes, and others that inflate their neck region as a defensive maneu- ver, a large saclike diverticulum of the left lung extends into the neck. Inflation of the sac causes the neck region to greatly expand. Although the lung is the primary organ of gas exchange in the sea snake (Pelamis platurus), this species can take up oxygen through the skin at rates up to 33 percent of its total standard oxygen uptake and excrete carbon dioxide at rates up to 94 percent of its total rate (Graham, 1974). Specially adapted lungs that extend back to the cloaca and tightly seal- ing, valvular nostrils allow sea snakes to remain submerged for 8 hours or more before surfacing (Cooke, 1991). Some lizards, such as the desert iguana (Dipsosaurus dor- salis) conserve a significant amount of water by exhaling air that is cooler than the body temperature (Murrish and Schmidt-Nielsen, 1970). The distal portion of the nasal pas- sageways forms a slight depression in which fluid secreted from the nasal salt gland accumulates, which assists in humidifying incoming air. As the fluid becomes more con- centrated, salts crystalize near the opening of the nares. The chuckwalla (Sauromalus), a desert lizard from southwestern North America, often seeks refuge in rocky crevices. By inflating its lungs, it wedges its body in place and defies efforts to remove it from its safe haven. Recent studies have shown that Sauromalus “uses the primitive, anamniote, buccal pumping respiration for defense, and the derived, amniote, aspiration mechanism for respiration” (Deban and Theimer, 1991). Buccal pumping, unlike aspi- ration, can create greater-than-ambient pressures in the abdominal cavity. Air sacs, which are diverticula of the lungs, extend among the viscera in some chameleons, often as far caudad as the pelvis (Orr, 1976). They serve to increase the air capac- ity and efficiency of the lungs in somewhat the same man- ner as the air sacs in birds. Although five pharyngeal pouches develop in reptilian embryos, gills never develop, and adults never have open gill slits. The first pharyngeal pouch persists in adults as the Eustachian (auditory) tube and middle ear, and in reptiles and birds this temporarily opens to the outside during embryonic development. The other pouches become mod- ified into other structures (thymus, parathyroid glands, and ultimobranchial body) or disappear during embryonic development. Digestive System The reptilian digestive tract exhibits numerous modifications as compared with amphibians. The jaws of most reptiles are covered by nonmuscular, immovable, thickened lips. The jaw margins of turtles, however, are covered with a shell of ker- atin and, together with the jaws, form a beak. [...]... 3, 284 2.9 Brain wt (g) 4.9 1.3 0.16 0.02 0.2 0.1 0.1 0.05 0.02 2.4 0.4 0.65 0.1 0.04 0.093 0.125 0.130 0. 08 0.043 3 .8 0. 48 12,000 1,360 29 0.125 Source: Data from A D Bellairs, The Life of Reptiles, 2 vols., 1970, © Universe Books Brain wt as % body wt 0.04 0.07 0.2 1.5 0. 08 0.2 0.2 0.2 0. 28 0.03 0.04 0.04 0.16 0.2 0.6 0.5 0.4 0.6 0.9 0.2 5.3 0.01 2.1 0.9 4.3 213 Linzey: Vertebrate Biology 214 8 Reptiles:... consists of a series of long-chain methyl ketones (Mason et al., 1 989 ) Females of related groups of snakes have some of the same methyl ketones as well as variations of the com- Linzey: Vertebrate Biology 8 Reptiles: Morphology, Reproduction, and Development © The McGraw−Hill Companies, 2003 Text Reptiles: Morphology, Reproduction, and Development FIGURE 8. 29 221 BIO-NOTE 8. 3 A Volcanic Nest In a study... concentration of the Linzey: Vertebrate Biology 2 18 8 Reptiles: Morphology, Reproduction, and Development © The McGraw−Hill Companies, 2003 Text Chapter Eight plasma becomes high In the orbit of each eye, marine turtles have a salt-excreting lacrimal gland A nasal gland performs a similar function in marine iguanas and some desert-dwelling lizards (Templeton, 1966) Sea snakes have a salt-excreting gland... triple-jointed, extremely mobile lower jaw of threadsnakes that allows the transversely oriented mandibular tooth rows (the only teeth in the skull) to be rotated backwards The high-speed gulping is thought to minimize the time spent in insect nests It is the only vertebrate feeding mechanism known in which prey is transported exclusively by movements of the lower jaw Linzey: Vertebrate Biology 8 Reptiles:... up formed elements (red blood cells, white blood cells, and platelets) in the blood and attack the lining of blood vessels Linzey: Vertebrate Biology 210 8 Reptiles: Morphology, Reproduction, and Development © The McGraw−Hill Companies, 2003 Text Chapter Eight FIGURE 8. 16 FIGURE 8. 17 Nostril Loreal pit Fang Opening to loreal pit Outer chamber Venom duct Venom gland Discharge orifice (a) Glottis Brain... column of the African egg-eating snake (Dasypeltus scaber) Anterior is to the left with the rear of the skull being shown Note vertebrae with thickened hypapophyses (ventral processes) used for crushing egg shells and those with long, anteriorly directed hypapophyses that slit the egg membranes Source: Pough, Herpetology, 19 98, Prentice-Hall, Inc Linzey: Vertebrate Biology 8 Reptiles: Morphology, Reproduction,... (Sphenodon) breed only once every Linzey: Vertebrate Biology 222 8 Reptiles: Morphology, Reproduction, and Development © The McGraw−Hill Companies, 2003 Text Chapter Eight 4 or 5 years and take 2 or 3 years to develop eggs After mating, eggs are held in the oviduct for another 7 months before they are deposited Twelve to 16 months later, the eggs finally hatch The 10-cm-long babies spend a few days in... long-term effects on posthatching survival, growth rates, behavior, and environmental preferences of some reptiles (Lang, 1 987 ; Burger, 1 989 ; Webb and Cooper-Preston, 1 989 ; Van Damme et al., 1992) To determine behavioral differences as a function of incubation temperature, pine snake (Pituophis melanoleucus) eggs were incubated at temperatures of 21, 23, 26, 28, 30, and 32°C Hatchlings from medium-temperature... Viperidae (Crotalus atrox) Viperidae (Agkistrodon piscivorus) FIGURE 8. 32 225 29 29 25 25 23 22 22 21 From Introduction to Herpetology, 3E by C J Goin, Goin, and Zug © 19 78 by W H Freeman and Company Used with permission Linzey: Vertebrate Biology 226 8 Reptiles: Morphology, Reproduction, and Development © The McGraw−Hill Companies, 2003 Text Chapter Eight age of 56 years, and several species of snakes,... the surface This middle transitional layer is equivalent to the stratum spinosum and stratum granulosum layers of mammals Linzey: Vertebrate Biology 230 8 Reptiles: Morphology, Reproduction, and Development © The McGraw−Hill Companies, 2003 Text Chapter Eight FIGURE 8. 37 FIGURE 8. 39 Barn owl feathers Long hairlike extensions of the barbules seen in this highly magnified scanning electron micrograph . shell of ker- atin and, together with the jaws, form a beak. Linzey: Vertebrate Biology 8. Reptiles: Morphology, Reproduction, and Development Text © The McGraw−Hill Companies, 2003 2 08 Chapter. 8. 9d). It provides for rapid travel over a smooth, (a) (b) pg Linzey: Vertebrate Biology 8. Reptiles: Morphology, Reproduction, and Development Text © The McGraw−Hill Companies, 2003 204 Chapter. their function of allowing side-to-side movement of the vertebral column, epaxial muscles take on new functions including support and Linzey: Vertebrate Biology 8. Reptiles: Morphology, Reproduction,