Turtle

This article is about the entire order of Chelonia/Testudines including tortoises and terrapins. For other uses, see Turtle (disambiguation).

Turtles Temporal range: Middle Jurassic – Present,
Florida box turtle (Terrapene carolina)
Scientific classification
Domain:	Eukaryota
Kingdom:	Animalia
Phylum:	Chordata
Class:	Reptilia
Clade:	Pantestudines
Clade:	Testudinata
Clade:	Perichelydia
Order:	Testudines Batsch, 1788 .
Subgroups
Cryptodira Pleurodira †Paracryptodira
Diversity
14 extant families with 356 species
Blue: sea turtles, black: land turtles
Synonyms
Chelonii Latreille 1800 Chelonia Ross and Macartney 1802

Turtles are reptiles of the order Chelonia /kɪˈloʊniə/ or Testudines /tɛˈstjuːdɪniːz/. They are characterized by a bony or cartilaginous shell, developed from their ribs, that acts as a shield. Testudines include both extant (living) and extinct species. Its earliest known members date from the Middle Jurassic. Among the turtles are included tortoises and terrapins.

Turtles are the only vertebrates with a complete shell. It is formed mainly of bone; the upper part is the domed carapace, while the underside is the flatter plastron. Its outer surface is covered in scales made of keratin, the material of hair and fingernails. The carapace bones develop from ribs which grow sideways and develop broad flanges that join up to cover the body. Many turtles migrate short distances seasonally; the sea turtles are the only reptiles that migrate long distances to lay their eggs on a favored beach, sometimes traveling thousands of kilometers to feed before returning to the beach where they were born. It is not known how they navigate, though they do have a magnetic sense.

Turtles are ectotherms—commonly called cold-blooded—meaning that their internal temperature varies according to the ambient environment. However, because of their high metabolic rate and adaptations to conserve heat, leatherback sea turtles have a body temperature noticeably higher than that of the surrounding water. Turtles are classified as amniotes, along with other reptiles, birds, and mammals. Like other amniotes, turtles breathe air and do not lay eggs underwater, although many species live in or around water.

Turtles have appeared in myths and folktales around the world. Some terrestrial and freshwater species are widely kept as pets. Turtles have been hunted for their meat, for use in traditional medicine, and for their carapaces. Marine turtles are often killed accidentally as bycatch in fishing nets. Turtle habitats around the world are being destroyed. As a result of these pressures, many species are threatened with extinction.

Naming and etymology

"Turtle" is a common name and may be used without knowledge of taxonomic distinctions. In particular, "turtle" may denote the order as a whole, as in North American usage, or a non-monophyletic form taxon within the order, or only aquatic species, as in British usage.

Animals in the order are often called chelonians by veterinarians, scientists, and conservationists. The name "Chelonia", now a synonym for the order, is based on the Greek word for "turtle", χελώνη chelone; Greek χέλυς chelys "tortoise" is used in the formation of names of many turtle taxa. The name of the order, "Testudines", is based on the Latin word for tortoise, testudo.

Anatomy and physiology

Size

The largest living species of turtle, and fourth largest reptile, is the leatherback turtle which can grow up to 2.7 m (8 ft 10 in) and weigh over 500 kg (1,100 lb). On land, the Galápagos tortoises have reached lengths of 1.87 m (6.1 ft), and weights of over 417 kg (919 lb). The largest known turtle was Archelon ischyros, a Late Cretaceous sea turtle up to 4.6 m (15 ft) long and estimated to have weighed around 2,200 kg (4,900 lb). The smallest living turtle is the speckled padloper tortoise of South Africa. It measures no more than 8 cm (3.1 in) in length, and weighs about 140 g (4.9 oz).

Shell

Main article: Turtle shell

Sagittal section of a tortoise skeleton

The shell of a turtle is unique among vertebrates and serves to protect the animal and provide shelter from the elements. It is primarily made of bone, and consists of two parts, the carapace which usually contains 50–60 bones and covers the back of the animal while the plastron has 7–11 bones and covers the belly. They are connected by lateral extensions of the plastron. The carapace is fused with the vertebrae and ribs while the plastron is formed from bones of the shoulder girdle, sternum, and gastralia (dermal bones). During development, the ribs grow sideways into the carapacial ridge, unique to turtles, entering the dermis of the back to support the carapace. The development is signaled locally by fibroblast growth factors including FGF10. The shoulder girdle in turtles is made up of two bones, the scapula and the procoracoid. Both the anterior and posterior pelvis of turtles are located within the shell and hence are effectively within the rib-cage; the trunk ribs grow over the shoulder girdle during development.

The outer surface of the shell is covered in epidermal scales known as scutes which are made of keratin, the same substance that makes up human hair and fingernails. Typically, a turtle has 38 scutes on the carapace and 16 on the plastron; 54 in total. Carapace scutes are divided into "marginals" around the margin, "vertebrals" over the vertebral column, in many species an extra singular scute between the first marginals called the "cervical" is present, and "costals" between the marginals and vertebrals. Plastron scutes include gulars (throat), humerals, abdominals, femorals and anals. The side necked turtles of the Pleurodira have an extra plastral scute called the "intergular." Turtle scutes usually interlock like mosaic tiles, though in some species, like the hawksbill sea turtle, the scutes on the carapace can overlap.

Development of the shell: seen in the egg at stage 16/17, the carapace is developing. In section, the ribs are growing sideways not downwards, into the carapacial ridge, seen here as a bud, to support the carapace.

The shapes of turtle shells vary with the adaptations of the individual species. and sometimes with gender. Land-dwelling turtles tend to have more domed shells, which appear to make them more resistant to being crushed by large animals. Aquatic turtles have flatter, smoother shells which allow them to cut though the water. Sea turtles in particular have streamlined shells which reduce drag and increase stability in the open ocean. Some turtle species have ridged, lumped, or spiked shells which provide extra protection from predators and camouflage against patterned backgrounds. The humps of a tortoise shell may tilt its body when it gets flipped over, allowing it to flip back. In male tortoises, the lead edge of the plastron is thickened; it is used for butting and ramming during combat.

Shells vary in flexibility. In tortoises, the plastron and its extensions lock the sides of the carapace together, giving it even greater crushing resistance. Some species, such as box turtles, lack the extensions and instead have the carapace bones fully fused or ankylosed together, creating a single unit. Several species have hinges on their shells, usually on the plastron, which allow them to expand and contract. Softshell turtles have rubbery edges, due to the loss of bones. The leatherback turtle has hardly any bones in its shell, which instead consists of thick connective tissue covered in leathery skin.

Jackson (2002) suggested that the turtle shell can function as a pH buffer. To endure through anoxic conditions, such as winter periods beneath ice or within anoxic mud at the bottom of ponds, turtles utilize two general physiological mechanisms: their shell releases carbonate as a buffer, and takes up lactic acid.

Head and neck

Skull of a sea turtle; unlike in other diapsid reptiles, turtles have no openings behind the eye socket.

The turtle's skull is unique among living amniotes; it is solid and rigid with no openings for muscle attachment (temporal fenestra). Muscles instead attach to recesses in the back of the skull. Living turtles also lack teeth but have a bony cusp that may be beak-like or have serrations. Cusps are covered in keratin which usually have a sharp edge for cutting and slicing. Turtle skulls vary in shape; from the elongated skulls of softshells to the broad and flattened skull of the mata mata. Some turtle species have developed proportionally large and thick heads, allowing for greater muscle mass and stronger bites. Turtles that are carnivorous or durophagous (eating hard-shelled animals), such as Mesoclemmys nasuta, have the most powerful bites, in its case 432 lbf (1,920 N); species that are insectivorous, piscivorous or omnivorous have lower bite forces.

The necks of turtles are highly flexible, possibly to compensate for their rigid shells. Some species, like sea turtles, have short necks while others, such as snake-necked turtles, have very long ones. Despite this, all turtle species have eight neck vertebrate; a consistency not found in other reptiles but paralleled in mammals. Some snake-necked turtles have both long necks and large heads and thus have difficulty lifting them when not in water.

Limbs and locomotion

Turtles are slow-moving on land, because of their heavy shells; a desert tortoise moves at only .22–.48 km/h (0.14–0.30 mph). By contrast, sea turtles can swim at 30 km/h (19 mph). The limbs of turtles are adapted for various means of locomotion and habits; most have five toes. Tortoises are specialized for terrestrial environments and have column-like legs with elephant-like feet with short toes. The gopher tortoise has flattened front-limbs for digging in the substrate. Aquatic turtles have more flexible legs and longer toes with webbing, getting them thrust in the water. Some of these species, such as snapping turtles and mud turtles, mainly walk along the water bottom, much as they would on land. Others, such as terrapins, swim by paddling with all four limbs with the simultaneous retraction of the opposing front and hind limbs, helping them maintain their direction while thrusting.

Sea turtles have streamlined shells and limbs adapted for fast and efficient swimming.

Sea turtles and the pig-nosed turtle are the most specialized for aquatic locomotion. Their front limbs have evolved into flippers while the shorter hind limbs are shaped more like rudders. The front limbs provide most of the thrust for swimming, while the hind limbs serve as stabilizers. Sea turtles such as Chelonia mydas rotate the front limb flippers like a bird's wings so as generate a propulsive force on both the upstroke and on the downstroke. This is in contrast to similar-sized freshwater turtles (measurements having been made on young animals in each case) such as Mauremys caspica, which use the front limbs like the oars of a rowing boat, creating substantial negative thrust on the recovery stroke in each cycle. In addition, the streamlining of the marine turtles reduces drag. As a result, marine turtles produce a propulsive force twice as large, and swim six times as fast, as freshwater turtles. The swimming efficiency of young marine turtles is similar to that of fast-swimming fish of open water, like mackerel.

Compared to other reptiles, turtles tend to have reduced tails, but these vary in both length and thickness among species and between sexes. They are especially large in snapping turtles and the big-headed turtle, the latter of which uses its tail to balance itself while climbing. The cloaca is at the base of the tail, and the tail itself houses the reproductive organs. Hence, males have longer tails to accommodate the penis. In sea turtles, the tail is longer and also somewhat prehensile; males use it to grasp females when mating. Several turtle species have spines on their tails.

Senses

The red-eared slider has an exceptional seven types of color-detecting cells in its eyes.

Turtles make use of vision to find food and mates, to avoid predators, and to orient themselves. The retina's light-sensitive cells include both rods for vision in low light, and cones with three different photopigments for bright light, where they have full color vision. There is possibly a fourth type of cone that detects ultraviolet; hatchling sea turtles respond experimentally to ultraviolet light, but it is unknown if they can distinguish this from longer wavelengths. A freshwater turtle, the red-eared slider, has an exceptional seven types of cone cell defined by the color of their oil droplets and their photopigments.

Sea turtles orient themselves on land by night, using visual features detected in dim light; they use their eyes in all conditions from clear surface water to muddy coasts and the darkness of the deep ocean, and with their heads above water. Unlike in terrestrial turtles, the cornea, the curved surface that lets light into the eye, does not help to focus light on the retina, so focusing underwater is handled entirely by the lens, behind the cornea. The cone cells contain oil droplets placed to shift perception towards the red part of the spectrum; this improves color discrimination. Visual acuity, studied in hatchlings, is highest in a horizontal band with retinal cells packed about twice as densely as elsewhere; this gives the best vision along the visual horizon. Sea turtles do not appear to use polarized light for orientation as many other animals do. The deep-diving leatherback turtle lacks specific adaptations to low light, such as large eyes, large lenses, or a reflective tapetum; it may rely on seeing the bioluminescence of prey when hunting in deep water.

Turtles have ear-structures inside their heads; they are sensitive to low tones around 100 Hertz, but their hearing fades away at higher frequencies and they are unable to hear tones above around 500 Hertz. Among sea turtles, the loggerhead has been shown experimentally to respond both by behavior and by evoked electrical signals to low sounds, with maximal sensitivity between 100 and 400 Hertz.

Like other vertebrates, turtles have an olfactory sense and an olfactory bulb in the brain. Experiments on green sea turtles showed they could learn to respond to a selection of different odorant chemicals (such as triethylamine and cinnamaldehyde) detected by olfaction in the nose. Such signals could be used in navigation.

Breathing

A submerged Indian softshell turtle nose-breathing at river surface

Although many turtles spend large amounts of their lives underwater, all turtles breathe air and must surface at regular intervals to refill their lungs. Immersion periods vary between a minute and an hour depending on the species. Some turtles spend much or all of their lives on dry land. Aquatic respiration in Australian freshwater turtles is currently being studied. Some species have large cloacal cavities that are lined with many finger-like projections. These projections, called papillae, have a rich blood supply and increase the surface area of the cloaca. The turtles can take up dissolved oxygen from the water using these papillae, in much the same way that fish use gills to respire.

Respiration, for many amniotes, is achieved by the contraction and relaxation of specific muscle groups (i.e. intercostals, abdominal muscles, and/or a diaphragm) attached to an internal rib-cage that can expand or contract the body wall thus assisting airflow in and out of the lungs. The ribs of turtles, however, are, uniquely, fused with their carapace and external to their pelvic and pectoral girdles. This rigid shell is not capable of expansion, so the turtles have had to evolve special adaptations for respiration. They ventilate their lungs using specific groups of abdominal muscles attached to their viscera and shell that pull the lungs ventrally during inspiration, where air is drawn in via a negative pressure gradient. In expiration, the contraction of the transversus abdominis muscle propels the viscera into the lungs and expels air under positive pressure. Conversely, the relaxing and flattening of the oblique abdominis muscle pulls the transversus back down which, once again, draws air back into the lungs. Important auxiliary muscles used for ventilatory processes are the pectoralis, which is used in conjunction with the transverse abdominis during inspiration, and the serratus, which moves with the abdominal oblique accompanying expiration.

The lungs of Testudines are multi-chambered and attached their entire length down the carapace. The number of chambers can vary between taxa, though most commonly they have three lateral chambers, three medial chambers, and one terminal chamber. As previously mentioned, the act of specific abdominal muscles pulling down the viscera (or pushing back up) is what allows for respiration in turtles. Specifically, it is the turtles large liver that pulls or pushes on the lungs. Ventral to the lungs, in the coelomic cavity, the liver of turtles is attached directly to the right lung, and their stomach is directly attached to the left lung by the ventral mesopneumonium, which is attached to their liver by the ventral mesentery. When the liver is pulled down, inspiration begins. Supporting the lungs is the post-pulmonary septum, which is thought to prevent the lungs from collapsing.

Circulation

Snapping turtle emerging from period of brumation, in which it buried itself in mud. Turtles have multiple circulatory and physiological adaptations to enable them not to breathe for long periods.

Turtles share the linked circulatory and pulmonary systems of vertebrates, where the heart pumps deoxygenated blood through the lungs, and then pumps the returned oxygenated blood through the body's tissues. The turtle cardiopulmonary system has both structural and physiological adaptations that distinguish it from other vertebrates. Turtles have a large lung volume; they can shunt blood through non-pulmonary blood vessels, including some within the heart, to avoid the lungs while they are not breathing; they can hold their breath for much longer periods than other reptiles; they can tolerate the resulting low oxygen levels; they can moderate the increase in acidity during anaerobic respiration by chemical buffering; and they can lie dormant for months, in aestivation or brumation.

The heart has two atria but only one ventricle. The ventricle is subdivided into three chambers; a muscular ridge enables a complex pattern of blood flow, so that the blood can be directed either to the lungs via the pulmonary artery, or to the body via the aorta. The ability to separate the two outflows varies between species; the leatherback has a powerful muscular ridge enabling almost complete separation of the outflows, supporting its actively swimming lifestyle, whereas the ridge is less well developed in freshwater turtles like the sliders (Trachemys).

Turtles are capable of longer periods of anaerobic respiration than many other vertebrates. This process breaks down sugars incompletely to lactic acid, rather than all the way to carbon dioxide and water as in aerobic respiration. They make use of the shell to buffer the increasing acidity of the body fluids that this causes.

Osmoregulation

Turtles have two or more accessory urinary bladders, located lateral to the neck of the urinary bladder and dorsal to the pubis, occupying a significant portion of their body cavity. The bladder is usually bilobed with a left and right section. The right section is located under the liver, which prevents large stones from remaining in that side while the left section is more likely to have calculi. Arid-living tortoises have bladders which serve as reserves of water; storing up to 20% of its body weight in fluids. The urine is normally very low in solutes. The bladder's wall is permeable, so when the animal becomes dehydrated, water returns by osmosis from the bladder to the blood, and the urine's solute concentration rises until it approaches that of the blood plasma. The fluids consist mainly of potassium ions from food plants.

To regulate the amount of salt in their bodies, sea turtles and diamondback terrapins secrete excess salt in a thick sticky substance from their lacrimal glands. When on land, sea turtles may appear to be "crying".

Thermoregulation

Smaller pond turtles, like these cooters (Pseudemys rubriventris), regulate their temperature by basking in the sun.

Turtles, like other reptiles, have a limited ability to regulate their body temperature; this varies between species, and with body size. Small pond turtles regulate their temperature by crawling out of the water and basking in the sun, while small terrestrial turtles move between sunny and shady places to adjust their temperature. Large species, both terrestrial and marine, have sufficient mass to give them substantial thermal inertia, meaning that they heat up or cool down over many hours. The Aldabra giant tortoise (Aldabrachelys gigantea) weighs up to some 60 kilograms (130 lb), and is able to allow its temperature to rise to some 33 Celsius on a hot day, and to fall naturally to around 29 Celsius by night. Some giant tortoises seek out shade to avoid overheating on sunny days. On Grand Terre Island, food is scarce inland, but shade is scarce near the coast, and the tortoises compete for space under the few trees on hot days; large males may push smaller females out of the shade, and some then overheat and die.

Adult sea turtles, too, have large enough bodies that they can to some extent control their temperature. The largest, the leatherback, can swim in the waters off Nova Scotia which may be as cool as 8 °C (46 °F); their body temperature has been measured at up to 12 °C (54 °F) warmer than the surrounding water. To help keep their temperature up, they have a system of countercurrent heat exchange in the blood vessels between their body core and the skin of their flippers; the vessels supplying the head are insulated by fat around the neck.

Behavior

Diet and feeding

A green sea turtle grazing on seagrass

Most turtle species are opportunistic omnivores; land-dwelling species being more herbivorous and aquatic ones being more carnivorous. Generally lacking speed and agility, most turtles feed either on plant material or on sedentary animals like mollusks, worms and insect larvae. Some species, such as the African helmeted turtle and snapping turtles, eat fish, amphibians, reptiles (including other turtles), birds and mammals; they may take them by ambush but also scavenge. The alligator snapping turtle has a worm-like appendage on this tongue which it uses to lure fish into its mouth. Tortoises are the most herbivorous group, consuming grasses, leaves, and fruits. Many turtle species, including tortoises, supplement their diet with eggshells, animal bones, hair and droppings for extra nutrients.

Turtles generally eat their food in a straightforward way, though some species have special feeding techniques. The yellow-spotted river turtle and the painted turtle filter feed by skimming the water surface with their mouth and throat open to collect particles of food. When the mouth closes, the throat constricts; excess water is pushed out through the nostrils and the gap in between the almost closed jaws. Some species, like the mata mata, employ a "gape-and-suck method" where the turtle opens its jaws and expands its throat widely, sucking the prey in.

The diet of an individual within a species may change with age, sex, and season, and may differ between populations. In many species, juveniles are generally carnivorous but become more herbivorous as adults. With Barbour's map turtle, the larger female mainly eats mollusks while the male eats mostly arthropods. Blanding's turtle may feed mostly on snails or crayfish depending on the population. The European pond turtle has been recorded being mostly carnivorous much of the year but switching to water lilies during the summer. Some species have developed specialized diets such as the Mekong snail-eating turtle, the hawksbill, which specializes on sponges, and the leatherback, which feeds on jellyfish.

Communication

The Arrau turtle has a sizable vocal repertoire.

While typically thought of as mute, turtles make various sounds when communicating. Tortoises may be vocal when courting and mating. Various species of both freshwater and sea turtles emit numerous types of calls, often short and low frequency, from the time they are in the egg to when they are adults. These vocalizations may serve to create group cohesion when migrating.

Migration

Turtles are the only reptiles that migrate long distances, up to thousands of kilometers in marine species; some non-marine turtles such as species of Geochelone (terrestrial), Chelydra (freshwater), and Malaclemys (estuarine) migrate seasonally over much shorter distances, up to around 27 kilometres (17 mi), to reach favored egg-laying sites. Such short migrations are comparable to those of some lizards, snakes, and crocodilians.

Both young and mature sea turtles undertake far longer migrations. They nest in a specific area, such as a beach, leaving the eggs to hatch unattended. The young turtles leave that area, migrating long distances in the years or decades in which they grow to maturity, and then return seemingly to the same area every few years to mate and lay eggs, though the precision varies between species and populations. This "natal homing" has appeared remarkable to biologists, though there is now plentiful evidence for it, including from genetics.

The mechanism by which sea turtles navigate to their breeding beaches remains unknown. One possibility is imprinting as in salmon, where the young learn the chemical signature, effectively the scent, of their home waters before leaving, and remember that when the time comes for them to return as adults. Another possible cue is the orientation of the earth's magnetic field at the natal beach; there is experimental evidence that turtles have an effective magnetic sense, and that they use this in navigation. Proof that homing occurs is derived from genetic analysis of populations of loggerheads, hawksbills, leatherbacks, and olive ridleys by nesting place; for each of these species, the populations in different places have their own mitochondrial DNA genetic signatures which persist over the years, showing that the populations are distinct, so that homing must be occurring reliably.

Defense

See also: Anti-predator adaptation

Crested caracara eating a turtle

When sensing danger, a turtle may flee, freeze or withdraw into its shell. Freshwater turtles flee into the water, though the Sonora mud turtle may take refuge on land as the shallow temporary ponds they inhabit make them more vulnerable. When startled, a softshell turtle may dive underwater and bury itself under the floor. If a predator persists, the turtle may bite or discharge from its cloaca. Several species produce foul-smelling chemicals from musk glands. Other tactics include threat displays and, in the case of Bell's hinge-back tortoise, playing dead. When attacked, big-headed turtle hatchlings squeal, possibly startling the predator.

Intelligence

See also: Animal cognition

Turtles have a very low encephalization quotient (relative brain to body mass), and their hard shells enable them to live without fast reflexes or elaborate predator avoidance strategies. Nevertheless, case studies exist of play behaviour in some turtle species. In the laboratory, turtles (Pseudemys nelsoni) can learn novel tasks and have demonstrated a long-term memory of at least 7.5 months. Similarly, giant tortoises can learn and remember tasks, and master lessons much faster when trained in groups. Tortoises appear to be able to retain operant conditioning nine years after their initial training.

Reproduction and lifecycle

Desert tortoises fighting

Turtles have a wide variety of mating behaviors, but do not form pair-bonds or social groups. Females generally outnumber males, as seen in green turtles, and as a result, most males copulate with multiple partners throughout their lifespan. Most terrestrial species are sexually dimorphic, with males larger than females; fighting between males often establishes a dominance hierarchy for access to food and mates, including in the Galápagos tortoise. For most semi-aquatic and bottom-walking aquatic species, combat occurs less often; males of these species instead often use their size advantage to mate forcibly. In fully aquatic species, males are often smaller than females, and rely on courtship displays to gain mating access to females.

Courtship and mounting

Courtship varies between species, and with habitat. In red-eared sliders, a fully aquatic species, the male courts the female by extending his forelegs with the palms facing out and fluttering his forelegs in the female's face. Female choice is important in this method, and the females of some species, such as green sea turtles, are not always receptive. As such, they have evolved behaviors to avoid the male's attempts at copulation, such as swimming away, confronting the male followed by biting, or taking up a refusal position with her body vertical, her limbs widely outspread, and her plastron facing the male. If the water is too shallow for the refusal position, the females resort to beaching themselves, as the males will not follow them ashore.

Mounting behavior in the radiated tortoise

All turtles fertilize internally; mounting and copulation can be difficult. In many species, males have a concave plastron that fits with the female's carapace. In species like the Russian tortoise, the male has a lighter shell and longer legs. The high, rounded shells of box turtles are particular obstacles for mounting; the male eastern box turtle leans backwards into position and hooks onto the back of the female's plastron. Aquatic turtles mount in water; female sea turtles support the mounting male while swimming and diving. During copulation, the male turtle forces his tail under the female's to allow for their cloacas to align and he can insert his penis. Some female turtles can store sperm from multiple males and their egg clutches can have multiple sires.

Forced copulation occurs in some species. The male scorpion mud turtle relies on overpowering females with its larger size. The male approaches the female from the rear, and often resorts to aggressive methods such as biting the female's tail or hind limbs, followed by a mounting. Male radiated tortoises use surrounding vegetation to trap or prevent females from escaping, then pin them down for copulation.

Eggs and hatchlings

eastern box turtle laying an egg

Turtles, including sea turtles, lay their eggs on land, although some lay eggs close to or in shallow water which rises and falls in level. While most species build nests and lay eggs where they forage, some travel miles. The common snapping turtle walks 5 km (3.1 mi) on land to lay eggs, while sea turtles travel even further; the leatherback swims some 12,000 km (7,500 mi) to its nesting beaches. Most turtles prepare a nest for their eggs; females usually dig a flask-like chamber in the substrate. Other species lay their eggs in vegetation or crevices. Females choose nesting locations based on environmental factors such as temperature and humidity, which are important for developing embryos. The number of eggs laid varies from 10 to over 100 depending on the species. Larger females can lay eggs that are greater in number or bigger in size. Compared to freshwater turtles, tortoises deposit fewer but larger eggs. Females can lay multiple clutches throughout a season, particularly in species that experience unpredictable monsoons.

Olive ridley sea turtle hatchlings heading to sea

Most mother turtles do no more in the way of parental care than covering their eggs and immediately leaving, though some species guard their nests for days or weeks. Eggs vary between spherical, oval and elongated and between hard- and soft-shelled. Most species have their sex determined by temperature; in some species, higher temperatures produce females and lower ones produce males, while in others, intermediate temperatures produce males and both hot and cold extremes produce females. There is experimental evidence that the embryos of Mauremys reevesii can move around inside their eggs to select the optimal temperature for development, thus influencing their sexual destiny. In other species, sex is determined genetically. The length of incubation for turtle eggs varies from two to three months for temperate species, and four months to over a year for tropical species. Species that live in warm temperate climates may go though embryonic diapause.

When ready to hatch, young turtles break out of the shell using a sharp projection on their upper beak. Hatchlings dig out of the nest and find cover in vegetation or water. Some species remain in the nest for longer, be it for overwintering or to wait for rain to soften the soil for them to dig out. Turtles are highly vulnerable to predators, both in the egg and as hatchlings. Mortality is high during this period but significantly decreases when they reach adulthood. Most species grow rapidly during their early years and slow down when they are mature.

Lifespan

Turtle can live very long lives; a Galápagos tortoise collected by Charles Darwin in 1835 died in 2006, living for at least 176 years though most wild turtles do not reach that age. Turtles keep growing new scutes under the previous scutes every year, allowing researchers to estimate how long they have lived; they age very slowly. The survival rate for adult turtles can reach 99 percent per year.

Systematics and evolution

Further information: Turtle classification and List of Testudines families

Fossil history

Diagram of origins of turtle body plan through the Triassic: isolated bony plates evolved to form a complete shell, in a sequence involving Pappochelys, Eorhynchochelys, Odontochelys, and Proganochelys.

Zoologists have sought to explain the evolutionary origin of the turtles, and in particular of their unique carapace. In 1914, J. Versluys proposed that bony plates in the dermis, osteoderms, fused to the ribs beneath them. The theory persisted into the 21st century, when Olivier Rieppel proposed a hypothetical turtle precursor, its back covered by bony armour plates in the dermis, which he called the "Polka Dot Ancestor". The theory accounted for the evolution of fossil pareisaurs from Bradysaurus to Anthodon, but not for how the ribs could have become attached to the bony dermal plates. Recent stem-turtle fossil discoveries provide a different but "comprehensive scenario" of the evolution of the turtle's shell. A fossil that may be a stem-turtle from the Permian of South Africa, Eunotosaurus, had a short broad trunk, and a body-case of broadened and somewhat overlapping ribs, suggesting an early stage in the acquisition of a shell.

A stem-turtle from the Middle Triassic, Pappochelys, has more distinctly broadened ribs, T-shaped in cross-section. A Late Triassic stem-turtle from Guizhou, China, Eorhynchochelys, is a much larger animal, up to 1.8 metres (5.9 ft) long, with a long tail, and broadened but not overlapping ribs; like the earlier fossils, it has small teeth. Also in the Late Triassic, the freshwater Odontochelys semitestacea of Guangling in southwest China has a partial shell, consisting of a complete bony plastron and an incomplete carapace. The development of a shell reaches completion with the late Triassic Proganochelys. It lacked the ability to pull its head into its shell, and had a long neck and a long, spiked tail ending in a club, somewhat like an ankylosaur.

Once a complete shell was in place, turtles underwent an adaptive radiation in the Jurassic, greatly increasing the number and diversity of fossil species. In a few places, paleontologists have unearthed large numbers of Jurassic or Cretaceous turtle skeletons accumulated in a single area, such as the Nemegt Formation in Mongolia, the Turtle Graveyard in North Dakota, the Black Mountain Turtle Layer in Wyoming, and in Shanshan County, Xinjiang, where over a thousand ancient freshwater turtles died after the last water hole in an area dried out during a major drought. Hatchling and nestling size fossils have been documented.

External phylogeny

The turtles' exact ancestry has been disputed. It was believed they are the only surviving branch of the ancient evolutionary grade Anapsida, which includes groups such as procolophonids, millerettids, protorothyrids, and pareiasaurs. All anapsid skulls lack a temporal opening while all other extant amniotes have temporal openings (although in mammals, the hole has become the zygomatic arch). The millerettids, protorothyrids, and pareiasaurs became extinct in the late Permian period and the procolophonoids during the Triassic.

It was later suggested that the anapsid-like turtle skull may be due to reversion rather than to anapsid descent. More recent morphological phylogenetic studies with this in mind placed turtles firmly within diapsids, slightly closer to Squamata than to Archosauria. All molecular studies have strongly upheld the placement of turtles within diapsids; some place turtles within Archosauria, or, more commonly, as a sister group to extant archosaurs, though an analysis conducted by Lyson et al. (2012) recovered turtles as the sister group of lepidosaurs instead. Reanalysis of prior phylogenies suggests that they classified turtles as anapsids both because they assumed this classification (most of them studying what sort of anapsid turtles are) and because they did not sample fossil and extant taxa broadly enough for constructing the cladogram. Testudines were suggested to have diverged from other diapsids between 200 and 279 million years ago, though the debate is far from settled. Even the traditional placement of turtles outside Diapsida could not be ruled out at that time. A combined analysis of morphological and molecular data conducted by Lee (2001) found turtles to be anapsids (though a relationship with archosaurs could not be statistically rejected). Similarly, a morphological study conducted by Lyson et al.. (2010) recovered them as anapsids most closely related to Eunotosaurus.

A 2012 molecular analysis of 248 nuclear genes from 16 vertebrate taxa suggests that turtles are a sister group to birds and crocodiles (the Archosauria). The date of separation of turtles and birds and crocodiles was estimated to be 255 million years ago. The most recent common ancestor of living turtles, corresponding to the split between Pleurodira and Cryptodira, was estimated to have occurred around 157 million years ago. The oldest definitive crown-group turtle (member of the modern clade Testudines) is Caribemys oxfordiensis from the late Jurassic period (Oxfordian stage). Through genomic-scale phylogenetic analysis of ultraconserved elements (UCEs) to investigate the placement of turtles within reptiles, Crawford et al. (2012) similarly suggest that turtles are a sister group to birds and crocodiles (Archosauria).

The first genome-wide phylogenetic analysis was completed by Wang et al. (2013). Using the draft genomes of Chelonia mydas and Pelodiscus sinensis, the team again concluded that turtles are likely a sister group of crocodilians and birds (Archosauria). This placement within the diapsids suggests that the turtle lineage once had a diapsid-like skull with temporal openings behind the eye socket, whereas turtles now possess an anapsid-like skull without such openings. The external phylogeny of the turtles is shown in the cladogram below.

Diapsida	Archosauromorpha Crocodilia (crocodiles, alligators) Aves (birds) Testudines Lepidosauromorpha Squamata (lizards, snakes)

Internal phylogeny

Thompson and colleagues comment that extant turtles have very low diversity, given the group's age. Diversity increased steadily in their analysis, speciation occurring at a greater rate than extinction, except for a single rapid increase around the Eocene-Oligocene boundary some 30 million years ago, and a major regional extinction at roughly the same time. They suggest that global climate change caused both events, as the cooling and drying caused land to become arid and turtles to become extinct there, while new continental margins exposed by the climate change provided habitats for other species to evolve. The cladogram, from Crawford et al. 2015, shows the internal phylogeny of the Testudines down to the level of families. The analysis by Thompson et al. 2021 supports the same structure down to family level.

Testudines

Pleurodira Pelomedusidae Podocnemididae Chelidae  (Side‑necked turtles)  Cryptodira Durocryptodira Testudinoidea Testudinidae (Tortoises) Geoemydidae Platysternidae Emydidae (Terrapins) Chelydroidea Chelydridae Dermatemydidae Kinosternidae Chelonioidea Dermochelyidae  (Leatherback)  Cheloniidae  (Sea turtles)  (Hardshell turtles) Trionychia Carettochelyidae  (Pig‑nosed turtle)  Trionychidae  (Softshell turtles)   (Hidden‑necked turtles)

Differences between the two suborders

Neck retraction

Cryptodira retract their necks backwards.

Pleurodira retract their necks sideways.

Turtles are divided into two extant suborders: Cryptodira and Pleurodira. Turtles in the two groups differ in the way the neck is retracted, and in the shape of the head. The Cryptodira is the larger group, and includes all the marine turtles, the terrestrial tortoises, and many of the freshwater turtles. The Pleurodira or side-necked turtles is a smaller group, consisting primarily of freshwater turtles. Until 3,000 years ago, there was a third group: the family Meiolaniidae was then extant, but it lay outside the Testudines crown group, belonging to Perichelydia.

The different mechanisms of neck retraction in the two suborders of turtles

Pleurodirans retract their neck laterally to the side, anterior to the shoulder girdles, whereas cryptodirans retract their neck back into their shell by bending the neck in an S-like shape. These motions are largely due to the morphology and arrangement of cervical vertebrae. The cervical column consists of nine joints and eight independent vertebrae. These vertebrae are round and not fused, making the neck more flexible and allowing it to bend backwards and sideways. The primary function and evolutionary implication of neck retraction is thought to be for feeding rather than protection. Neck retraction and extension allow the turtle to reach out further to capture prey while swimming. Neck extension creates suction when the head is thrust forward and the oropharynx is expanded. This morphology suggests the retraction function is for feeding purposes, as the suction helps catch prey.

The shape of the head differs between the two suborders, as the jaw musculature is associated with different bones in the two groups. The adductor muscles in the lower jaw create a pulley-like system in both subgroups; however the bone in which the muscles articulate with differ. In Pleurodira, the pulley is formed with the pterygoid bones, but in Cryptodires the pulley is formed with the quadrate bones. Both of these systems help to vertically redirect the adductor muscles in order to create a powerful bite.

Distribution and habitat

Turtles are widely distributed across the world's continents and oceans, being absent mainly from the polar regions, the northern parts of North America and Eurasia, and the driest regions of the Sahara, Arabia and Australia. There are terrestrial, fully aquatic, and semi-aquatic species, and within those realms they live in a wide range of habitats from pelagic (open ocean) to rivers, ponds, rainforest and deserts. Individual species have much narrower habitat preferences, so that few ecoregions have more than 5 species living together.

The two major groups of turtles have different distributions and habitat ranges. The Pleurodira are all semi-aquatic or fully aquatic, and are found only in the Southern Hemisphere. The Cryptodira include terrestrial, freshwater and marine species; these are found across the Northern Hemisphere, and in South America and Africa within the Southern Hemisphere.

Richest regions

The world regions richest in turtle species are the Amazon basin, the Southeastern United States, the coastal countries of tropical West Africa, and an extended area of South and Southeast Asia from the Himalayas to Bengal, Myanmar and Thailand to the Malay peninsula, Sumatra, the island of Borneo, Cambodia, Vietnam, and the southern coastal area of China (the south of Guangxi and Guangdong provinces).

Habitat range

Some turtles are found at high altitude; for example, the species Terrapene ornata occurs up to 6,600 feet (2,000 m) in New Mexico. Conversely, the leatherback sea turtle, Dermochelys coriacea, can dive to 4,100 feet (1,200 m). The desert tortoises, Gopherus spp. can tolerate body temperatures from below freezing to at least 104 °F (40 °C), though they are inactive (remaining in their burrows) at the lowest and highest temperatures.

Conservation

Many turtles have been killed accidentally in fishing nets. Some trawlers now use nets fitted with turtle excluders; seen here, a loggerhead escapes a net so fitted.

With between 48 and 54% of all 328 species considered threatened, turtles are at a much higher risk of extinction than many other vertebrates. Of the 263 species of freshwater and terrestrial turtles, 117 species are considered threatened, 73 are either endangered or critically endangered, and 1 is extinct. Of the 58 species in the family Testudinidae, 33 are threatened, 18 are either endangered or critically endangered, 1 is extinct in the wild, and 7 are extinct. 71% of all tortoise species are either gone or almost gone. Asian species are the most endangered, closely followed by the five endemic species of Madagascar. Turtles face many threats, including habitat destruction, harvesting for consumption, the pet trade, light pollution, and climate change. The high extinction risk for Asian species is primarily due to their long-term unsustainable exploitation for consumption and traditional Chinese medicine, and to a lesser extent for the international pet trade. Turtle extinction is progressing much faster than during the Cretaceous-Tertiary extinction; at the current rate, all turtles could be extinct in less than a century.

Turtle hatcheries can be set up when protection against flooding, erosion, predation or heavy poaching is required. Chinese entrepreneurs have sought to satisfy increasing demand for turtle meat as gourmet food and traditional medicine with farmed turtles, instead of wild-caught ones; according to a 2007 study, over a thousand turtle farms operated in China. Turtle farms in Oklahoma and Louisiana raise turtles for export to China. All the same, wild turtles continue to be caught and sent to market in large number (as well as to turtle farms, to be used as breeding stock, resulting in what conservationists have called "the Asian turtle crisis". In the words of the biologist George Amato, the hunting of turtles "vacuumed up entire species from areas in Southeast Asia", even as biologists still did not know how many species lived in the region. About 75% of Asia's 90 tortoise and freshwater turtle species are considered threatened. In 2000, all the Asian box turtles (Cuora spp.) were placed on the CITES list of endangered species.

Harvesting wild turtles is legal in some American states; most of the catch is exported to Asia. The Florida Fish and Wildlife Conservation Commission estimated in 2008 that around 3,000 pounds of softshell turtles were exported each week via Tampa International Airport. However, the great majority of turtles exported from the US are farmed.

Large numbers of marine turtles are accidentally killed in the nets of fishing trawlers as bycatch. A 2010 study suggested that over 8 million had been killed in 20 years; the Eastern Pacific and the Mediterranean were identified as among the areas worst affected. In 1987, the United States required all shrimp trawlers to fit their nets with turtle excluder devices; these have bars preventing turtles from being swept into the back of the net and drowning. More locally, other human activities are affecting marine turtles. In Australia, Queensland's shark culling program, which uses shark nets and drum lines, has since 1962 killed over 5,000 turtles as bycatch. The program has killed 719 loggerhead turtles and 33 critically endangered hawksbill turtles. New South Wales's shark control program has similarly killed at least 5,000 turtles.

Human uses

World Turtle

Further information: World Turtle and Turtle Island (Native American folklore)

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  4th century sculpture of turtle avatar of Vishnu. Garhwa, India
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  The 7th century Uttana Kurmasana, upside-down turtle pose, named for the avatar of Vishnu
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  World resting on four elephants on the back of the World Turtle. Western depiction of "The Hindu Earth", 1877

In Hindu mythology, the World Turtle, named Kurma or Kacchapa, supports four elephants on his back; they in turn carry the weight of the whole world on their backs. The turtle is one of the ten avatars or incarnations of the god Vishnu. The 7th century hatha yoga pose Uttana Kurmasana is named for the avatar.

World Turtles are found in Native American cultures including the Algonquian, Iroquois, and Lenape. They tell many versions of the creation story of Turtle Island. One version has Muskrat pile up earth on Turtle's back, creating the continent of North America. An Iroquois version has the pregnant Sky Woman fall through a hole in the sky between a tree's roots, where she is caught by birds who land her safely on Turtle's back; the Earth grows around her. The turtle here is altruistic, but the world is a heavy burden, and the turtle sometimes shakes itself to relieve the load, causing earthquakes.

A "cosmic turtle" and the island motif reappear in Gary Snyder's 1974 novel Turtle Island, and again in Terry Pratchett's Discworld series as A'Tuin the Great, starting with the 1983 novel The Colour of Magic; it is supposedly of the species Chelys galactica, the galactic turtle, complete with four elephants on its back to support Discworld.

In culture

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  Babylonian Kudurru with turtle (top), symbol of the god Enki, c. 1100 BC
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  Turtles (in basket) and other seafood in a fishmonger's shop by Bartolomeo Passerotti, 1580s
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  Bixi supporting Kangxi Emperor's stele, Beijing, 1698
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  Sea turtle in Aboriginal rock art, 1600–1900
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  The Mock Turtle in Lewis Carroll's 1865 Alice's Adventures in Wonderland
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  Poster for 1898 production of The Turtle at the Manhattan Theatre, Broadway
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  Terrapin shell leg rattles worn by lead Cherokee woman dancer, 20th century

Turtles have featured in human cultures across the world since ancient times. A turtle was the symbol of the Ancient Mesopotamian god Enki, from the 3rd millennium BC onwards. An ancient Greek origin myth told that only the tortoise refused the invitation of the gods Zeus and Hera to their wedding, as it preferred to stay at home; Zeus ordered it to carry its house with it, ever after. Another of their gods, Hermes, invented a seven-stringed lyre named the chelys or "tortoise"; its domed back was made of tortoiseshell. Other cultures too used turtle shells to make music: Native American shamans made them into ceremonial rattles, while Aztecs, Mayas and Mixtecs made ayotl drums. In China, the turtle was one of the four sacred animals in Confucianism, while in the Han period, steles were mounted on top of stone turtles, later linked with Bixi, the turtle-shelled son of the Dragon King. Marine turtles feature significantly in Australian Aboriginal art.

The army of Ancient Rome used the testudo ("tortoise") formation in battles, especially sieges; it consisted of a tight pack of infantry, their shields held overhead to form a shield wall like the interlocking scutes of a tortoise's shell. In Aesop's Fables, "The Tortoise and the Hare" tells how an unequal race may be won by the slower partner.

Lewis Carroll's 1865 Alice's Adventures in Wonderland features a Mock Turtle, named for a soup meant to imitate the expensive soup made from real turtle meat. In 1896, the French playwright Léon Gandillot wrote a comedy in three acts named La Tortue; it was "a Parisian sensation" in its run in France, and came to the Manhattan Theatre, Broadway, New York in 1898 as The Turtle. More recently, turtles have featured in comic books and animations such as of the 1984 Teenage Mutant Ninja Turtles. Since the start of the 20th century, people in North America have organized turtle races, sometimes with children riding them.

As pets

A pet red-eared slider basking on a floating platform under a sun lamp

Some turtles, particularly small terrestrial and freshwater species, are kept as pets. They are seen by some people as cheap pets that need little care, underestimating the complexity and expense of proper turtle and tortoise husbandry. In Europe, turtle keeping became popular in the 1960s and 1970s, when large numbers of wild-caught turtles and tortoises were imported; this was especially devastating to the Mediterranean tortoise population. In the 1980s the import of wild-caught tortoises started to be banned in various countries. Most turtles and tortoises for sale in Europe today are captive-bred. In the United States, because of the risk of contracting salmonellosis through casual contact with turtles, it is illegal to sell turtles under 4 inches (10 cm) long as pets; but many stores and flea markets exploit a loophole which allows turtles under 4 in (100 mm) to be sold for educational purposes.

As food and other uses

The flesh of turtles, calipash or calipee, has long been considered a delicacy in Asian cultures, while turtle soup was once a prized dish in Anglo-American cuisine. Gopher tortoise stew has been popular with some groups in Florida. Fat from turtles is used in the Caribbean and in Mexico as a main ingredient in cosmetics, marketed under its Spanish name crema de tortuga. The supposed aphrodisiac or medicinal properties of turtle eggs created a large trade for them in Southeast Asia. Turtle plastrons are widely used in traditional Chinese medicine; Taiwan imports hundreds of tons of plastrons every year. A popular medicinal preparation based on herbs with or without powdered turtle plastron is guilinggao jelly. Real tortoiseshell, usually from the hawksbill turtle, has been used for centuries to make jewellery, tools and ornaments around the Western Pacific. It was widely used around the world, including in Europe, until the trade was banned by international treaty in 2014. The material, often imitated with other materials, was sliced thinly to manufacture practical and decorative items such as combs, spectacle frames, furniture inlays, and guitar picks.

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  Catching turtles in Australia, 1875
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  Turtles on sale as food in Canada, 2007
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  Turtle plastrons for traditional Chinese medicine
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  A tortoiseshell comb; the material was expensive and decorative, and widely used for small items.

References

General sources

• Franklin, Carl J. (2011). Turtle: A Extraordinary Natural History 245 Million Years in the Making. Crestline. ISBN 978-0-7858-2775-7.
• Orenstein, Ronald (2012). Turtles, Tortoises and Terrapins: a Natural History. Richmond Hill, Ontario: Firefly Books. ISBN 978-1-77085-119-1. OCLC 791162481.
• Pryke, Louise (2021). Turtle. London: Reaktion Books. ISBN 978-1-78914-336-2. OCLC 1223025640.

External links

• Turtle Survival Alliance
• Turtle Conservancy
• Biogeography and Phylogeny of the Chelonia (taxonomy, maps)
• New Scientist article (including video) on how the turtle evolved its shell
• Symposium on Turtle Evolution