Odors are carried to Jacobson’s organ by the tongue.
Characteristics and Natural History of Reptilian Orders
Anapsid Reptiles: Subclass Anapsida Turtles: Order Testudines
Turtles descended from one of the earliest anapsid lineages, probably a group known as procolophonids of the late Per- mian, but turtles themselves do not appear in the fossil record until the Upper Triassic, some 200 million years ago. From the Triassic, turtles plodded on to the present with very little change in their early morphology. They are enclosed in shells consisting of a dorsal carapace(Fr., from Sp.carapacho,cov- ering) and ventral plastron (Fr., breastplate). Clumsy and unlikely as they appear to be within their protective shells, they are nonetheless a varied and ecologically diverse group that seems able to adjust to human presence. The shell is so much a part of the animal that it is fused to thoracic vertebrae
and ribs (figure 18.6). Like a medieval coat of armor, the shell offers protection for the head and appendages, which, in most turtles, can be retracted into it. But because the ribs are fused to the shell, the turtle cannot expand its chest to breathe.
Instead, turtles employ certain abdominal and pectoral mus- cles as a “diaphragm.” Air is drawn inward by contracting limb flank muscles to make the body cavity larger. Exhalation is also active: the shoulder girdle is drawn back into the shell, thus compressing the viscera and forcing air out of the lungs.
The terms “turtle,” “tortoise,” and “terrapin” are applied variously to different members of the turtle order. In North American usage, they are all correctly called turtles. The term “tortoise” is frequently given to land turtles, especially large forms. British usage of the terms is different:“tortoise”
is the inclusive term, whereas “turtle” is applied only to the aquatic members.
Lacking teeth, turtle jaws are provided with tough, horny plates for gripping food (figure 18.7). Sound perception is poor in turtles, and most turtles are mute (the biblical “voice of the turtle” refers to the turtledove, a bird). Compensating for poor hearing is a good sense of smell and color vision. Turtles are oviparous, and fertilization is internal. All turtles, even marine forms, bury their shelled, amniotic eggs in the ground.
An odd feature of turtle reproduction is that in some turtle families, as in all crocodilians and some lizards, nest tempera- ture determines sex of the hatchlings. In turtles, low tempera- tures during incubation produce males and high temperatures produce females.
Marine turtles, buoyed by their aquatic environment, can reach great size. Leatherbacks are largest, attaining a length of 2 m and weight of 725 kg. Green turtles, so named because of their greenish body fat, may exceed 360 kg, although most individuals of this economically valuable and heavily exploited species seldom live long enough to reach anything approach- ing this size. Some land tortoises may weigh several hundred kilograms, such as the giant tortoises of the Galápagos Islands (figure 18.8) that so intrigued Darwin during his visit there in 1835. Most tortoises are rather slow moving; one hour of deter- mined trudging carries a large Galápagos tortoise approxi- mately 300 m. A low metabolism probably explains in part the longevity of turtles, for some are believed to live more than 150 years.
Diapsid Reptiles: Subclass Diapsida
Diapsid reptiles, that is, reptiles having a skull with two pairs of temporal openings (see figure 18.2), are classified into three lineages (superorders; see the Classification of Living Reptiles on p. 354). The two with living representatives are superorder Lepidosauria, containing lizards, snakes, worm lizards, and Sphenodon;and superorder Archosauria, containing crocodil- ians (and birds in cladistic taxonomy).
Lizards, Snakes, and Worm Lizards:
Order Squamata
Squamates are the most recent and diverse products of diapsid evolution, approximately 95% of all known living reptiles.
Lizards appeared in the fossil record as early as the Permian, but they did not begin their radiation until the Cretaceous period of the Mesozoic when the dinosaurs were at the climax of their radiation. Snakes appeared during the late Cretaceous period, probably from a group of lizards whose descendants include the Gila monster and monitor lizards. Two specializations in particular characterize snakes: extreme elongation of the body with accompanying displacement and rearrangement of inter- nal organs; and specializations for eating large prey.
The diapsid skulls of squamates are modified from the ancestral diapsid condition by loss of dermal bone ventral and posterior to the lower temporal opening. This modification has allowed the evolution in most lizards of a kinetic skull having movable joints (figure 18.9). The quadrate, which in other reptiles is fused to the skull, has a joint at its dorsal end, as well as its usual articulation with the lower jaw. In addition, there are joints in the palate and across the roof of the skull that allow the snout to be tilted upward. The specialized mobility of the skull enables squamates to seize and manipu- late their prey. It also increases the effective closing force of the jaw musculature. The skull of snakes is even more kinetic than that of lizards. Such exceptional skull mobility is consid- ered a major factor in diversification of lizards and snakes.
Lizards: Suborder Sauria Lizards are an extremely diverse group, including terrestrial, burrowing, aquatic, arboreal and aerial members. Among the more familiar groups in this varied suborder are geckos(figure 18.10), small, agile, mostly noctur- nal forms with adhesive toe pads that enable them to walk upside down and on vertical surfaces;iguanas,often brightly colored New World lizards with ornamental crests, frills, and throat fans, and a group that includes the remarkable marine iguana of the Galápagos Islands (figure 18.11);skinks,with elongate bodies and reduced limbs; and chameleons,a group of arboreal lizards, mostly of Africa and Madagascar.
Chameleons are entertaining creatures that catch insects with a sticky-tipped tongue that can be flicked accurately and rapidly to a distance greater than the length of their body (fig- ure 18.12). The great majority of lizards have four limbs and relatively short bodies, but in many the limbs are degenerate,
Plastron
Carapace Fused vertebrae
Ribs
Neck
f i g u r e 18.6
Skeleton and shell of a turtle, showing fusion of vertebrae and ribs with the carapace. The long and flexible neck allows the turtle to withdraw its head into its shell for protection.
f i g u r e 18.7
Snapping turtle,Chelydra serpentina,showing the absence of teeth.
Instead, the jaw edges are covered with a horny plate.
f i g u r e 18.8
Mating Galápagos tortoises. Males have a concave plastron that fits over the highly convex carapace of females, helping to provide stability during mating. Males utter a roaring sound during mating, the only time they are known to emit vocalizations.
and a few such as the glass lizards (figure 18.13) are com- pletely limbless.
Unlike turtles, snakes, and crocodilians, which have dis- tinctive body forms and ways of life, lizards have radiated extensively into a variety of habitats and reveal an array of functional and behavioral specializations. Most lizards have movable eyelids, whereas a snake’s eyes are permanently cov- ered with a transparent cap. Lizards have keen vision for day-
light (retinas rich in both cones and rods), although one group, the nocturnal geckos, has retinas composed entirely of rods for night vision. Most lizards have an external ear that snakes lack.
However, as with other reptiles, hearing does not play an important role in the lives of most lizards. Geckos are excep- tions because the males are strongly vocal (to announce terri- tory and discourage the approach of other males), and they must, of course, hear their own vocalizations.
Quadrate Quadrate
Pterygoid Pterygoid
Lower temporal opening
Upper jaw
Lower jaw Lower jaw
f i g u r e 18.9
Kinetic diapsid skull of a modern lizard (monitor lizard,Varanussp.) showing the joints that allow the snout and upper jaw to move on the rest of the skull. The quadrate can move at its dorsal end and ventrally at both the lower jaw and the pterygoid. The front part of the braincase is also flexible, allowing the snout to be raised. Note that the lower temporal opening is very large with no lower border; this modification of the diapsid condition, common in modern lizards, provides space for expansion of large jaw muscles. The upper temporal opening lies dorsal and medial to the postorbital-squamosal arch and is not visible in this drawing.
f i g u r e 18.10
Tokay,Gekko gecko,of Southeast Asia has a true voice and is named after the strident repeated to-kay, to-kaycall.
f i g u r e 18.11
A large male marine iguana,Amblyrhynchus cristatus,of the Galápagos Islands, feeding underwater on algae. This is the only marine lizard in the world. It has special salt-removing glands in the eye orbits and long claws that enable it to cling to the bottom while feeding on small red and green algae, its principal diet. It may dive to depths exceeding 10 m (33 feet) and remain submerged more than 30 minutes.
f i g u r e 18.12
A chameleon snares a dragonfly. After cautiously edging close to its tar- get, the chameleon suddenly lunges forward, anchoring its tail and feet to the branch. A split second later, it launches its sticky-tipped, foot-long tongue to trap the prey. The eyes of this common European chameleon (Chamaeleo chamaeleon) are swiveled forward to provide binocular vision and excellent depth perception.
Many lizards have successfully invaded the world’s hot and arid regions, aided by characteristics that make desert life possible. Because their skin lacks glands, water loss by this avenue is much reduced. They produce a semisolid urine with a high content of crystalline uric acid, a feature well suited for conserving water also found in other groups that live success- fully in arid habitats (birds, insects, and pulmonate snails).
Some, such as the Gila monster of the southwestern United States deserts, store fat in their tails, which they use during drought to provide both energy and metabolic water (figure 18.14). Many lizards keep their body temperature relatively constant by behavioral thermoregulation.
Worm Lizards: Suborder Amphisbaenia The somewhat inappropriate common name “worm lizards”describes a group of highly specialized, burrowing forms that are neither worms nor true lizards but certainly are related to the latter. They have elongate, cylindrical bodies of nearly uniform diameter, and most lack any trace of external limbs (figure 18.15). With soft skin divided into numerous rings, and eyes and ears hidden under skin, amphisbaenians superficially resemble earth- worms—a kind of structural convergence that often occurs when two very distantly related groups come to occupy simi- lar habitats. Amphisbaenians have an extensive distribution in South America and tropical Africa.
Snakes: Suborder Serpentes Snakes are entirely limbless and lack both pectoral and pelvic girdles (the latter persists as a vestige in pythons and boas). The numerous vertebrae of
f i g u r e 18.13
A glass lizard,Ophisaurussp., of the southeastern United States. This leg- less lizard feels stiff and brittle to the touch and has an extremely long, fragile tail that readily fractures when the animal is struck or seized.
Most specimens, such as this one, have only a partly regenerated tip to replace a much longer tail previously lost. Glass lizards can be readily distinguished from snakes by the deep, flexible groove running along each side of the body. They feed on worms, insects, spiders, birds’ eggs, and small reptiles.
f i g u r e 18.14
Gila monster,Heloderma suspectum,of southwestern United States desert regions and the related Mexican beaded lizard are the only venomous lizards known. These brightly colored, clumsy-looking lizards feed principally on birds’ eggs, nesting birds, mammals, and insects. Unlike venomous snakes, the Gila monster secretes venom from glands in its lower jaw. The chewing bite is painful to humans but seldom fatal.
f i g u r e 18.15
A worm lizard of suborder Amphisbaenia. Worm lizards are burrowing forms with a solidly constructed skull used as a digging tool. The species pictured,Amphisbaena alba,is widely distributed in South America.
The Mesozoic World of Dinosaurs • • •
hen, in 1841, the English anato- mist Richard Owen coined the term dinosaur(“terrible lizard”) to describe fossil Mesozoic reptiles of gigan- tic size, only three poorly known dinosaur genera were distinguished. But with new and marvelous fossil discoveries quickly follow- ing, by 1887 zoologists were able to distin- guish two groups of dinosaurs based on differences in the structure of the pelvic gir- dles. The Saurischia (“lizard-hipped”) had a simple, three-pronged pelvis with hip bones arranged much as they are in other reptiles. A large bladelike ilium is attached to the back- bone by stout ribs. The pubis and ischium extend ventrally and posteriorly, respectively, and all three bones meet at the hip socket, a deep opening on the side of the pelvis. The Ornithischia (“bird-hipped”) had a somewhat more complex pelvis. The ilium and ischium were arranged similarly in ornithischians and saurischians, but the ornithischian pubis was a narrow, rod-shaped bone with anteriorly and posteriorly directed processes lying alongside the ischium. Oddly, while the ornithischian pelvis, as the name suggests, was similar to that of birds, birds are of the saurischian lineage.
Dinosaurs and their living relatives, the birds, are archosaurs (“ruling lizards”), a group that includes thecodonts (early archosaurs restricted to the Triassic), crocodilians, and pterosaurs (refer to the classification of the reptiles on p. 354). As traditionally recognized, dinosaurs are a paraphyletic group because they do not include birds, which are descended from the most recent common ancestor of dinosaurs.
From among the various archosaurian radiations of the Triassic there emerged a the- codont lineage with limbs drawn under the body to provide an upright posture. This lin- eage gave rise to the earliest dinosaurs of the Late Triassic. In Herrerasaurus, a bipedal dinosaur from Argentina, we see one of the
most distinctive characteristics of dinosaurs:
walking upright on pillarlike legs, rather than on legs splayed outward as with modern amphibians and reptiles. This arrangement allowed legs to support the great weight of the body while providing an efficient and rapid stride.
Although their ancestry is unclear, two groups of saurischian dinosaurs have been proposed based on differences in feeding habits and locomotion: the carnivorous and bipedal theropods, and the herbivorous and quadrupedal sauropods (sauropodomorphs).
Coelophysis was an early theropod with a body form typical of all theropods: powerful hindlegs with three-toed feet; long, heavy counterbalancing tail; slender, grasping fore- limbs; flexible neck; and a large head with jaws armed with daggerlike teeth. Large predators such as Allosaurus,common dur- ing the Jurassic, were replaced by even more massively built carnivores of the Cretaceous, such as Tyrannosaurus, which reached a length of 14.5 m (47 ft), stood nearly 6 m high, and weighed more than 7200 kg (8 tons). Not all predatory saurischians were massive; several were swift and nimble, such as Velociraptor (“speedy predator”) of the Upper Cretaceous.
Herbivorous saurischians, the quadru- pedal sauropods, appeared in the Late Trias- sic. Although early sauropods were small- and medium-sized dinosaurs, those of the Jurassic and Cretaceous attained gigantic proportions, the largest terrestrial vertebrates ever to have lived.Brachiosaurusreached 25 m (82 ft) in length and may have weighed in excess of 30,000 kg (33 tons). Even larger sauropods have been discovered;Supersauruswas 43 m (140 ft) long. With long necks and long front legs, the sauropods were the first vertebrates adapted to feed on trees. They reached their greatest diversity in the Jurassic and began to decline in overall abundance and diversity during the Cretaceous.
The second group of dinosaurs, the Ornithischia, were all herbivorous. Although more varied, even grotesque, in appearance than saurischians, ornithischians are united by several derived skeletal features that indi- cate common ancestry. The huge back-plated Stegosaurusof the Jurassic is a well known example of armored ornithischians which comprised two of the five major groups of ornithischians. Even more shielded with bony plates than stegosaurs were the heavily built ankylosaurs, “armored tanks” of the dinosaur world. As the Jurassic gave way to the Cretaceous, several groups of unarmored ornithischians appeared, although many bore impressive horns. The steady increase in ornithiscian diversity in the Cretaceous paral- leled a concurrent gradual decline in giant sauropods, which had flourished in the Juras- sic.Triceratops is representative of horned dinosaurs that were common in the Upper Cretaceous. Even more prominent in the Upper Cretaceous were the duck-billed dinosaurs (hadrosaurs) which are believed to have lived in large herds. Many hadrosaurs had skulls elaborated with crests that proba- bly functioned as vocal resonators to pro- duce species-specific calls.
Sixty-five million years ago, the last of the Mesozoic dinosaurs became extinct, leaving birds and crocodilians as the only surviving archosaurs. There is increasingly convincing evidence that the demise of dinosaurs coin- cided with the impact on earth of a large asteroid that produced devastating world- wide environmental upheaval. We continue to be fascinated by the awe-inspiring, often staggeringly large creatures that dominated the Mesozoic era for 165 million years—an incomprehensibly long period of time. Today, inspired by clues from fossils and footprints from a lost world, scientists continue to piece together the puzzle of how the various dino- saur groups arose, behaved, and diversified.
W
ORNITHISCHIANS SAURISCHIANS
CRETACEOUSJURASSICTRIASSIC
Titanosaurus 12 m (40 ft)
Velociraptor 1.8 m (6 ft)
Brachiosaurus 25 m (82 ft)
Allosaurus 11 m (35 ft)
Coelophysis 3 m (10 ft)
Hadrosaur (duck-billed dinosaur) 10 m (33 ft)
Herrerasaurus 4 m (13 ft) One of the oldest known dinosaurs. Has characteristics of both saurischians and ornithischians.
Triceratops 9 m (30 ft)
Stegosaurus 9 m (30 ft)
Ilium
Ischium
Pubis
Ilium Ischium Pubis 65
MYBP*
136 MYBP*
190 MYBP*
275
MYBP* *Millions of years before present
snakes, shorter and wider than those of legged vertebrates, permit quick lateral undulations through grass and over rough terrain. Ribs increase rigidity of the vertebral column, provid- ing more resistance to lateral stresses. The elevation of the neural spine gives the numerous muscles more leverage.
In addition to the highly kinetic skull that enables snakes to swallow prey several times their own diameter (figure 18.16), snakes differ from lizards in having no movable eyelids (snakes’ eyes are permanently covered with upper and lower transparent eyelids fused together) and no external ears. Most snakes have relatively poor vision, tree-living snakes of the tropical forest being a conspicuous exception (figure 18.17).
In fact, some arboreal snakes possess excellent binocular vision, which they use to track prey through branches where scent trails would be difficult to follow. Snakes are totally deaf, although they are sensitive to low-frequency vibrations con- ducted through the ground.
Nevertheless, most snakes employ chemical senses rather than vision or vibration detection to hunt their prey. In addition to the usual olfactory areas in the nose, which are not well developed, snakes have a pair of pitlike Jacobson’s organsin the roof of the mouth. These organs are lined with an olfactory epithelium and are richly innervated. The forked tongue, flicked through the air, picks up scent particles (figure 18.18);
the tongue is then drawn past Jacobson’s organs. Information is transmitted from Jacobson’s organs to the brain, where scents are identified.
Snakes of subfamily Crotalinae within family Viperidae are called pit vipersbecause they possess special heat-sensi- tive pit organson their heads, located between their nostrils and eyes (figures 18.18, 18.19, and 18.20). All of the best- known North American venomous snakes are pit vipers, such as the several species of rattlesnakes, water moccasins, and copperheads. The pits are supplied with a dense packing of free nerve endings from the fifth cranial nerve. They are exceedingly sensitive to radiant energy (long-wave infrared) and can distinguish temperature differences smaller than 0.003°C from a radiating surface. Pit vipers use their pits to track warm-blooded prey and to aim strikes, which they can make as effectively in total darkness as in daylight.
All vipers have a pair of teeth, modified as fangs, on the maxillary bones. The fangs lie in a membranous sheath when the mouth is closed. When a viper strikes, a special muscle and bone lever system erects the fangs as the mouth opens (figure 18.20). Fangs are driven into prey by the thrust, and venom is injected into the wound through a canal in the fangs. A viper immediately releases its prey after the bite and follows it until it is paralyzed or dies. Then the snake swallows the prey whole. Approximately 8000 bites but only 12 deaths from pit vipers are reported each year in the United States.
f i g u r e 18.16
Black rat snake,Elaphe obsoleta obsoleta,swallowing a chipmunk.
f i g u r e 18.17
Parrot snake,Leptophis ahaetulla.The slender body of this Central American tree snake is an adaptation for sliding along branches without weighting them down.
f i g u r e 18.18
A blacktail rattlesnake,Crotalus molossus,flicks its tongue to smell its surroundings. Scent particles trapped on the tongue’s surface are trans- ferred to Jacobson’s organs, olfactory organs in the roof of the mouth.
Note the heat-sensitive pit organ between the nostril and eye.