Amniote Evolution PDF

The amniotes are a group of tetrapod vertebrates that include reptiles, birds and mammals, all of which are characterised by the possession of an amniotic egg. Amniote embryos whether laid as eggs or carried by the female, are protected and aided by several extensive membranes. In humans, these memb...

The amniotes are a group of tetrapod vertebrates that include reptiles, birds and mammals, all of which are characterised by the possession of an amniotic egg. Amniote embryos whether laid as eggs or carried by the female, are protected and aided by several extensive membranes. In humans, these membranes include the amniotic sac that surrounds the foetus. The first amniotes, which resembled small lizards, evolved 340 million years ago. Their eggs could survive out of water and could also 'breathe' and cope with waste, allowing the eggs and the resultant juvenile and adult forms to evolve into larger forms. The amniotes spread across the globe and became the dominant land vertebrates. Amniotes are defined by embryonic development that includes the formation of several extensive membranes, the amnion, chorion, and allantois. Amniotes develop directly into a (typically) terrestrial form with limbs and a thick stratified epithelium, rather than first entering a feeding larval tadpole stage followed by metamorphosis, as in amphibians. The unique embryonic features of amniotes may reflect specialisations of eggs to survive drier environments, or the massive size and yolk content of eggs designed for direct development to a larger size. 1. Eggshell 3. Inner membrane 2. Outer membrane 4. Chalaza 5. Exterior albumen (outer thin albumen) 6. Middle albumen (inner thick albumen) 7. Vitelline membrane 8. Nucleus of Pander 9. Germinal disk (blastoderm) 10. Yellow yolk 11. White yolk 12. Internal albumen 13. Chalaza 15. Cuticula 14. Air cell Features of amniotes designed for survival on land include a sturdy but porous leathery or hard eggshell, and an allantois designed to facilitate respiration while providing a reservoir for the disposal of wastes. Most mammals do not lay eggs, but corresponding structures may be found inside the placenta. The first amniotes, such as Casineria kiddi, which lived about 340 million years ago, resembled small lizards. Their eggs were small and covered with a membrane, not a hard shell like most modern amniote eggs. This kind of egg only became possible with internal fertilisation. The outer membrane, a soft shell, evolved as a protection against the harsher environments on land, as species evolved to lay their eggs on land where they were safer than in the water. In amniotes, the inner anatomy of the egg has evolved further and new structures have developed to take care of the gas exchanges between the embryo and the atmosphere, as well as dealing with the waste problems. In order to grow a thicker and tougher shell, new ways to supply the embryo with oxygen had to be developed, as diffusion alone was not enough. After the egg had developed these structures, further sophistication allowed the amniotes to lay much bigger eggs in much drier habitats. Increasing body size lead to a diet change from relying on small invertebrates as their main food source and starting to eat plants or other vertebrates, or returning to the water. New habits and heavier bodies meant further evolution for the amniotes, both in behaviour and in anatomy. There are three main lines of amniotes, which may be distinguished by the structure of the skull and, in particular, the number of temporal fenestrae (openings) behind the eye. In anapsids (turtles), there are none, in synapsids (mammals and their extinct relatives) there is one, and in most diapsids (non-anapsid reptiles, dinosaurs, and birds) there are two. Introduction class Reptilia Members of class reptilia include the first truly terrestrial vertebrates. There are thought to be nearly 8000 living species occupying a wide variety of habitats both aquatic and terrestrial. However, despite their current diversity, they are still noted, because of what they once were. The age of reptiles, lasting over 165 million years, saw a huge radiation of reptilian forms, with herbivorous and carnivorous dinosaurs reaching sizes unknown on land today and only exceeded by the modern blue whale. During the mass extinction at the end of the Palaeozoic era, a huge variety of reptilian lineages disappeared, leaving the groups we see today. One of these groups, the tuataras (Sphenodon) is the sole survivor of a large group, which otherwise disappeared 100 million years ago. Understanding the 300 million year history of the reptiles is made complicated by widespread convergent and parallel evolutionary trends, and by large gaps in the fossil record. Origin of reptiles Most palaeontologists agree that amniotes arose from a group of amphibian-like tetrapods (the anthracosaurs) during the early carboniferous period of the Palaeozoic era. By the late carboniferous period, (300 mya) amniotes had separated into three distinct groups. The first group, anapsids, were characterised by having a skull without temporal openings behind the orbits, the skull is completely roofed with dermal bone. Today, this group is represented only by Chelonians (turtles, terrapins, tortoises). Their morphology is a mixture of ancestral and derived characteristics that is largely the same as that seen in the fossil record in the Triassic (200 million years ago). The second group, the diapsids, includes all other reptilian groups and birds, and are characterised by two pairs of temporal openings, one pair located low on the cheeks, and the second above the lower pair, and separated by a bony arch. Four subgroups of diapsids appeared; the leipidosaurs including all modern reptiles except the chelonians and crocodilians, the archosaurs comprising the dinosaurs, living crocodilians and birds, the suaropterygians including several aquatic extinct groups, e.g. plesiosaurs, and finally, the ichthyosaurs, extinct dolphin-like forms. The third main group, the synapsids comprise the mammals and mammal-like extinct reptiles. They were characterised by a single pair of temporal openings, low on the cheek. Synapsids were the first amniotes to diversify, giving rise to the pelycosaurs, later to the therapsids, and finally to the mammals. As usually defined, class reptilia excludes birds, which are descended from the most recent common ancestor of the reptiles. Consequently, reptiles are a prophylactic group (they do not include all descendants of their most recent common ancestor). The evolutionary tree below shows the relationships between reptilian groups, the section on 'ruling reptiles' (which includes early birds) will be expanded later in the module. Reptiles and birds share several characteristics, including skull morphology and aglandular skin with beta keratin (harder than normal keratin). Although it is recognised that Class reptilia is not a monophyletic group, it is useful as a convenient term to refer to all amniotes that have beta keratin in their epidermis that are not birds. Thus, 'reptiles' is used to refer to living turtles, snakes, lizards, tuatara, crocodilians, and extinct groups such as plesiosaurs, ichthyosaurs, pterosaurs and dinosaurs. Crocodilians and birds are sister groups, as they are more recently descended from a common ancestor rather than either form being from any other living reptilian group. They are referred to as Archosauria, a group that also contains the extinct dinosaurs. In some systems, birds are included in class reptilia, others justify their placement in a separate class by referring to their novel adaptations and grade of organisation and this system will be used in this module. Distinguishing reptiles from amphibians 1. Reptiles have tough, dry, scaly skin, which provides protection from injury and desiccation. Reptilian skin consists of a thin epidermis and a much thicker, well-developed dermis. The epidermis is characterised by a complete covering of beta keratin in the form of scales, which provide protection against physical wear. In addition, the epidermis contains hydrophobic lipids, which prevent desiccation. It also contains chromatophores, (colour bearing cells, which give lizards and snakes their wide-ranging colour variations). The characteristic scales of reptiles are not homologous to fish scales, (which are bony and dermal in origin) as they are derived mostly from the epidermis. In some reptiles (crocodilians), scales remain throughout life, growing gradually to replace wear. In others, (snakes and lizards) ecdysis occurs when the mitosis in the lower skin layers form new cells, which move up, and the old outer layer is shed. Crocodiles and many lizards also possess bony plates (ectoderms), which are located beneath the stratum corneum in the dermis. The chelonian shell is covered with living tissue composed of keratinised epidermis covering the underlying dermal plate, which is the chelonian's vertebrae and rib cage. 2. The amniotic egg of reptiles permits rapid development of large young in relatively dry environments. Features of the amniotic egg have been discussed previously in this module. 3. Reptilian jaws are efficiently designed for applying crushing or gripping force to prey. Jaws of fishes and amphibians are designed for quick closure. However, once prey is seized, little static force can be applied. Reptilian jaws have larger, longer muscles arranged for maximum mechanical advantage. 4. Reptiles have some from of copulatory organ, which permits internal fertilisation. Internal fertilisation is necessary with the production of shelled eggs. Sperm must reach the egg before it is enclosed. Sperm from paired testes are carried by the vas deferentia to a copulatory organ (penis or hemipenes, an invagination of the cloacal wall). The female system consists of paired ovaries and oviducts. Glandular walls of the oviducts secrete albumin (source of amino acids, minerals and water for the embryo), and shell. 5. Reptiles have an efficient and flexible circulatory system and higher blood pressure than amphibians. In all reptiles, the right atrium (receiving deoxygenated blood from the body) is completely partitioned from the left atrium, which receives oxygenated blood from the lungs. Crocodilians additionally have two completely separate ventricles. In other groups, the ventricle is incompletely partitioned into multiple chambers. Even in reptiles with incompletely separated ventricles, flow patterns within the heart prevent mixing of oxygenated (pulmonary) and deoxygenated (systemic) blood. This means that all reptiles have functionally two separate circulatory systems, as do birds and mammals. The incomplete separation between the left and right sides of the heart in most reptiles has the advantage of permitting blood to bypass the lungs when pulmonary respiration is not occurring (e.g. when diving). 6. Reptilian lungs are better developed than those of amphibians. Reptiles depend almost exclusively on lungs for respiration (some aquatic turtles can supplement via pharyngeal membranes). Unlike amphibians, which force air into their lungs with mouth muscles, reptiles more efficiently suck in air by enlarging their thoracic cavity (by either expanding the ribcage as in snakes and lizards, or by movement of internal organs as in turtles and crocodilian). Reptiles have no muscular diaphragm, which is found only in mammals. Amphibians use cutaneous respiration (across skin membranes) to a great extent, a practice abandoned by the reptiles. 7. Reptiles have evolved efficient strategies for water conservation. All amniotes have a metamorphic kidney, which is drained by a ureter. However, the nephrons of the reptilian kidney lack the specialised section of the tubule (the loop of Henle), which enables a mammalian kidney to concentrate solutes in urine. As an alternative, many reptiles have salt glands located near the nose or eyes (in the tongue of saltwater crocodiles), which secrete a salty fluid. Nitrogenous wastes are excreted as uric acid, rather than urea or ammonia. Uric acid has a low solubility and precipitates out of solution readily allowing water to be conserved. As a result, the urine of many reptiles is a semi-solid suspension. 8. All reptiles (except limbless species) have better body support than amphibians and have limbs more efficiently adapted for terrestrial movement. Nevertheless, most modern reptiles walk with their legs splayed out, and the underside close to the ground. On the other hand, most dinosaurs (and some modern lizards) walked upright on legs held beneath the body, which is the best arrangement for rapid movement and support of body weight. Many dinosaurs were, in addition, bipeds. Reptilian nervous systems are considerably more complex than amphibian systems. Although the reptile brain is small, the cerebrum is relatively large compared to the rest of the brain. Connections within the central nervous system are more advanced allowing behaviours far in advance of those possible for amphibians. With the exception of hearing, sense organs of reptiles are well developed. Reptiles (particularly lizards and snakes) possess the Jacobson's organ (specialised olfactory organ), with odours transferred to the organ in the roof of the mouth by the tongue. Mesozoic reptiles (dinosaurs) The term, 'dinosaur' was first used by the English anatomist, Richard Owen, in 1841 to describe fossil Mesozoic reptiles of enormous size. Only three poorly known dinosaurs were generally distinguished. However, a plethora of fossil discoveries followed in the next decades. By 1887, zoologists were able to categorise findings into one of two groups based on pelvic girdle structures. The Saurischia (lizard hipped) species had a simple three pronged pelvis with hips arranged much like modern reptiles. The large blade like ilium is attached to the backbone by stout ribs. The pubis and ischium extend interiorly and ventrally 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 are located somewhat similar to the batrachians, but the ornithischian pubis was a narrow rod- shaped bone with interiorly and posterior directed processes lying alongside the ischium. Interestingly, although the ornithischian pelvis was similar to modern birds, birds are decedents of the sacrischian lineage. Dinosaurs and their living relatives (the birds) are archosaurs (ruling lizards) a group, which contains thecodonts (Triassic dinosaurs), crocodiles and pterosaurs. The dinosaurs are considered to be a prophylactic group, as they do not contain birds, which are descended from the most recent common ancestor of dinosaurs. From amongst the various arch saurian radiations of the Triassic (see evolutionary tree), emerged a homodont line with limbs drawn up under the body, providing an upright stance. This line gave rise to the earliest dinosaurs of the late Triassic. hind limbs. Herrerasaurus is considered to be one of the first dinosaurs, having both characteristics of sacristans and ornithischians. Herrerasaurus was a lightly built bipedal carnivore with a long tail and a relatively small head. Its length is estimated at 3m to 6m, its hip height at 1.1m, and it weighed around 210kg--350kg. It had relatively short forelimbs that were less than half the length of its The first two fingers and the thumb bore curved, sharp claws for grasping prey. Its fourth and fifth digits were small stubs without claws. This genus was probably one of the first dinosaurs to adopt the distinctive bipedal theropod-like shape, as it had strong hind limbs with short thighs and rather long feet, indicating that it was most likely a swift runner. The balancing tail, partially stiffened by overlapping vertebral processes, also indicates an adaptation for speed. The teeth of Herrerasaurus indicate it was carnivorous, its size indicates prey were small and medium-sized animals. It may have fed on other dinosaurs, such as the herbivorous Pisanosaurus. However, since Herrerasaurus lived during an era when other dinosaurs were uncommon, more plentiful prey would have included rhynchosaurs and aetosaurs. Herrerasaurus itself may have been preyed upon by giant rauisuchids-like Saurosuchus, as puncture wounds were found in one skull. Coprolites (fossilized dung) containing small bones, but no trace of plant fragments, have been assigned to Herrerasaurus indicating the ability to digest bones. Studies suggest that the paleoenvironment was a volcanically active floodplain covered by forests and subject to strong seasonal rainfalls. Vegetation consisted of ferns, sphenopsids (horsetails), and giant conifers. Herbivores were much more abundant than carnivores. These non-dinosaurian herbivores such as rhynchosaurs (Hyperodapedon); aetosaurs; kannemeyeriid dicynodonts (Ischigualastia), and traversodontids (Exaeretodonwere) were much more abundant than early ornithischian dinosaurs, and therefore more likely prey for Herrerasaurus than were early dinosaurs. Although their ancestry is unclear, two groups of saurischian dinosaurs have been proposed based on locomotion and feeding differences. The theropods were carnivorous and bipedal, and the sauropods were herbivorous and quadrapedal. These are classified as two suborders: Theropoda and Sauropodomorpha Theropods (\'beast feet\') are a group of bipedal saurischian dinosaurs. Although they were primarily carnivorous, a number of theropod families evolved herbivory during the Cretaceous Period. Theropods first appeared during the Carnian age of the Late Triassic about 220 million years ago, and were the sole large terrestrial carnivores from the Early Jurassic until the close of the Cretaceous, about 65 million years ago. The earliest and most primitive unambiguous theropods were the Coelophysidae. The Coelophysidae (Coelophysis, Megapnosaurus) were a group of widely distributed, lightly built and apparently gregarious animals. They included small hunters like Coelophysis and larger (6m) predators like Dilophosaurus. These successful animals continued from the Late Carnian (early late Triassic) through to the Toarcian (late early Jurassic). During the late Jurassic, there were no fewer than four distinct lineages of theropods - ceratosaurs, megalosaurs, carnosaurs, and coelurosaurs - preying on the abundance of small and large herbivorous dinosaurs. All four groups survived into the Cretaceous. Of all the theropod groups, the coelurosaurs were the most diverse. Some coelurosaur clades that flourished during the Cretaceous are: tyrannosaurs, the dromaeosaurs (Velociraptor), which are remarkably similar in form to the oldest known bird, Archaeopteryx, the omnivorous oviraptorosaurs, the omnivorous ornithomimids (\"ostrich dinosaurs\") and Therizinosauridae (giant-clawed herbivores) and the birds. While the roots of these various groups must have been in the Late or possibly even the middle Jurassic, they only became abundant during the early Cretaceous. Currently, the largest of all the known predatory dinosaurs (16m to 18m in length and nine tonnes in weight) belonged to this group. Spinosaurus (meaning 'spine lizard') lived in what is now North Africa, in the Cretaceous Period, about 100 to 93 million years ago. The distinctive 'spines' of Spinosaurus, which were long extensions of the vertebrae, grew up to 2m long and were likely to have had skin connecting them, forming a sail-like structure, although some authors have suggested that they were covered in muscle forming a hump or ridge. Functions for this structure could have included thermoregulation and display. The environment inhabited by Spinosaurus is only partially understood, and covers a great deal of what is now northern Africa. They may have contended with shoreline conditions on tidal flats and channels, living in mangrove forests alongside similarly large dinosaurian predators, the giant titanosaur sauropod Paralititan, the 10m long crocodilian Stomatosuchus, and the coelacanth Mawsonia. It is unclear whether Spinosaurus was primarily a terrestrial predator or a fisher, as indicated by its elongated jaws, conical teeth and raised nostrils. However, a tooth found embedded in a South American pterosaur bone suggests that spinosaurs occasionally preyed on these flying archosaurs. Spinosaurus was likely to have been a generalised and opportunistic predator, possibly a Cretaceous equivalent of a grizzly bear. The Spinosaurus sail is possibly analogous (not homologous) to that of the Permian mammal-like reptile, Dimetrodon, which lived before the dinosaurs even appeared; these similarities are due to parallel evolution. If the sail contained abundant blood vessels, the animal could have used the sail\'s large surface area to absorb heat. This would imply that the animal was only partly warm-blooded and lived in climates where night temperatures were cool and the sky usually clear. It is also possible that the sail was used to radiate excess heat from the body, rather than to collect it. Large animals, due to the relatively small ratio of surface area of their body compared to the overall volume (Haldane\'s principle), face far greater problems of dissipating excess heat at higher temperatures than gaining it at lower. Sails of these dinosaurs added considerably to the skin area of the body, with minimum increase of volume. If the sail was turned away from the sun, or positioned at a 90-degree angle towards a cooling wind, the animal would quite effectively cool itself in the warm climate of Cretaceous Africa. It is also possible that the sails were used for courtship, in a way similar to a peacock\'s tail. If this was the case, the sails may have been brightly coloured, but this is purely speculative. Finally, it is quite possible that the sail combined these functions, acting normally as a heat regulator, becoming a courting aid during the mating season, being used to cool itself and, on occasions, turning into an intimidating device when an animal was feeling threatened. The sauropodomorphs were a suborder saurischian ('lizard-hipped') dinosaur. They were the largest animals ever to have lived on land. Well-known genera include Apatosaurus (formerly known as Brontosaurus), Brachiosaurus and Diplodocus. Sauropods first appeared in the late Triassic Period, By the late Jurassic (150 million years ago) sauropods were widespread. By the late Cretaceous, only the titanosaurians survived, though with a near-global distribution. However, as with all other non-avian dinosaurs, the titanosaurians died out in the Cretaceous-Tertiary extinction event. Sauropodomorphs were adapted to higher browsing than any of its contemporaries. This feeding strategy is supported by many defining characteristics, e.g. a light, tiny skull on the end of a long neck (with ten or more elongated cervical vertebrae), a counterbalancing long tail (with one to three extra sacral vertebrae). Teeth were weak, shaped like leaves or spoons (lanceolate or spatulate), and they had stomach stones (gastroliths), similar to the gizzard stones of modern birds and crocodiles, to help digest tough plant fibres. The earliest known sauropodomorph, Saturnalia, was small and slender (1.5m long). At the end of the Triassic, they were the largest dinosaurs of their time, but later species dwarfed them. Ultimately, the largest sauropods like the Supersaurus, Diplodocus hallorum, and Argentinosaurus reached 30m--40m in length, and 60,000kg--100,000kg or more in weight. The early sauropodomorphs were most likely omnivores, as their shared common ancestor with the other saurischian lineage (the theropods) was a carnivore. Therefore, their evolution to herbivory went hand in hand with their increasing size, neck length, and move from bipedalism to a four footed mode of locomotion. Like all non-avian dinosaurs, the sauropodomorphs became extinct 65 million years ago, during the Cretaceous-Tertiary extinction event. Argentinosaurus was probably the heaviest at 80 to 100 tonnes, among the largest land animals that ever lived. It developed on the island continent of South America during the middle of the Cretaceous Period (100 million years ago), after all of its more familiar Jurassic kin (e.g. Apatosaurus) had long disappeared. The second main group of dinosaurs, the Ornithischia, were all herbivores. The huge back plated Stegosaurus of the Jurassic period is a well-known example of the armoured ornithischians. Stegosaurus was the largest stegosaur, reaching up to 12m in length and up to 5,000kg. Stegosaurus is considered to have been quadrapedal, but there has been discussion over whether it could have reared up on its hind legs, using its tail to form a tripod with its hind limbs, and browsing for higher foliage. Soon after Stegosaurus was first described, a large canal in the hip region of the spinal cord was noted, which could have accommodated a structure up to 20 times larger than the brain. This has led to the famous idea that dinosaurs like Stegosaurus had a \'second brain\' in the tail, which may have been responsible for controlling reflexes in the rear portion of the body. It has also been suggested that this 'brain' might have given a Stegosaurus a temporary boost when it was under threat from predators. More recently, it has been argued that this space (also found in sauropods) may have been the location of a glycogen body, a structure in living birds whose function is not definitely known, but which is postulated to facilitate the supply of glycogen to the animal\'s nervous system. The steady increase in ornithischian species numbers paralleled a concurrent decline in giant sauropods. Triceratops is representative of the honed dinosaurs present in the Upper Cretaceous, it was one of the last dinosaur genera to appear before the great Cretaceous--Tertiary extinction event. Bearing a large bony frill and three horns, Triceratops is one of the most recognisable of all dinosaurs, although it shared the landscape with, and was preyed upon by, the fearsome Tyrannosaurus; it is unclear whether the two battled the way they are commonly depicted in the media. The function of their frills and three distinctive facial horns have traditionally been viewed as defensive, other theories claim it is more probable that these features were used in courtship and dominance displays. Evidence that visual display was important, either in courtship or in other social behaviour, can be seen from the fact that horned dinosaurs differ markedly in their adornments, making each species highly distinctive. In addition, modern living creatures with such displays of horns and adornments use them in similar behaviour e.g. the antlers and horns of modern reindeer, mountain goats, or rhinoceros beetles. Even more prominent during the Upper Cretaceous were the hadrosaurs (duck-billed dinosaurs) e.g. Parasaurolophus, which were believed to have lived in large herds. Many hadrosaurs had skulls elaborated with crests that may have functioned as vocal resonators to produce species-specific calls. Hadrosaurs had a rudimentary dental specialisation analogous to incisors and molars. This has been hypothesised to be a crucial factor in the success of this group in the Cretaceous, compared to the sauropods, which were still largely dependent on gastroliths for grinding their food. Dinosaurs as a group probably had considerably more complex parental care than most other reptilian groups. Support for this theory can be established by examining the phylogenetic relationships of archosaurs. The two living groups, crocodilians and birds, have well-developed parental care, and the discovery of fossilised nests with attending adults, suggests that dinosaurs also exhibited parental care. One young hadrosaur was found at a nest site with worn teeth, suggesting food was brought to the youngster whilst it was in the nest. 75 million years ago, the Mesozoic dinosaurs became extinct, leaving birds as the only descendants of archosaurs. The extinction event coincided with a large asteroid impact in the Yucatan peninsula that would have produced a worldwide environmental disaster. However, the impact hypothesis does not explain why dinosaurs became extinct whilst other vertebrate lines did not. Many palaeontologists believe that changing climates and landforms at the close of the Cretaceous caused the extinctions. Modern reptiles Order Chelonia (testudines) Turtles descended from one of the earliest anapsid lineages, probably the procolophids of the late Permian period, although turtles themselves do not appear in the fossil record until the upper Triassic (around 200 million years ago). Today, the group is little changed from these examples. Characteristics of the group include the body being enclosed in a shell, consisting of a dorsal carapace, and a ventral plastron. The shell is composed of two layers, an outer horny layer of keratin and an inner bone layer. New keratin layers form beneath the old as the turtle grows and ages. The bony layer is a fusion of ribs, vertebrae and dermally ossified elements. Unique amongst vertebrates, turtle limbs and limb girdles are located inside the ribs. Lacking teeth, a turtle's jaw has tough, horny plates for gripping food. The main disadvantage of living in a fixed shell is that chelonians cannot expand their chests to breathe. They solve this problem by having abdominal and pectoral muscles as a diaphragm. Air is drawn in by increasing abdominal cavity volume, by contracting limb and flank muscles, exhalation is also an active process, drawing the shoulder girdle back into the shell, compressing the viscera and forcing air out of the lungs. Many aquatic forms obtain oxygen by pumping water in and out of a secularised mouth, enabling them to spend long periods of time underwater if inactive. The brain is small (never more than 1% of body weight), although having a cerebrum larger than amphibians allows a terrestrial chelonian to learn a maze at about the same speed as a rat. Turtles have a poor sense of hearing, but acute smell, vision and colour perception. Turtles are oviparous, fertilisation is internal, and all species (even marine) bury their eggs. An unusual feature of some species (and some crocodilians) is that nest temperature controls the sex of the embryos. In turtles, lower temperatures produce males, higher, females, and these species lack sex chromosomes.