Crocodilians

(Crocodiles, alligators, caimans, and gharials)

Class Reptilia

Order Crocodylia

Number of families 3

Number of genera, species 8 genera; 23 species

Evolution and systematics

There are 23 widely recognized species of crocodiles, alligators, caimans, and gharials, all members of the order Crocodylia. Superficially they resemble reptiles, yet their closest cousins are birds and extinct Dinosauria, a group known as archosaurs ("ruling reptiles"). Modern Crocodylia are the latest iteration of the Crocodylomorpha, a major group whose evolutionary heritage spans almost 240 million years. Crocodylia are often described as "living fossils," unchanged in millions of years, but this description is inaccurate. The Crocodylomorpha were a diverse and successful group occupying terrestrial, freshwater, and marine ecosystems, and their modern counterparts are barely less fantastic. This group is informally referred to as "crocodilians," although the term "crocodylians" technically refers to members of the order.

Every successful group has a beginning. The earliest crocodyliforms were terrestrial hunters that shared an ankle with modern Crocodylia, but little else, yet they were dominant predators whose legacy diversified throughout the Jurassic and Cretaceous periods. Their success is evident in excavations, as more crocodyliform material than dinosaur bones often turns up. Discoveries have been remarkable, such as curious peglike teeth and spiked protective plates from Desmatosuchus that indicate a defensive, vegetarian lifestyle. Despite dabbling in herbivory, it was in carnivory that crocodyliforms excelled. The awe-inspiring skulls of Sarcosuchus and Deinosuchus paint a picture of massive killers over 35 ft (10.7 m) in length. From terrestrial beginnings, crocodyliforms branched out into freshwater and marine habitats. In extreme thalattosuchians (marine crocodiles), limbs were replaced with paddles and a fluked tail to compete with sharks and ichthyosaurs for dominance of the sea. However, these marine forms were an evolutionary dead end, and freshwater species with limited marine ability proliferated from the Jurassic onward. Modern Crocodylia first appeared over 100 million years ago, and despite experiments with various and occasionally bizarre forms, the semiaquatic predator has become their signature role.

Scientists disagree about crocodyliform classification and evolutionary relationships. In 2003, 23 species of Crocodylia are widely recognized, divided into three families: Alligatoridae (alligators and caimans; eight species), Crocodylidae (crocodiles; 14 species), and Gavialidae (gharial; one species). The Crocodylidae are further divided into two subfamilies, Crocodylinae and Tomistominae. Some taxonomists also divide Alligatoridae into two subfamilies: Alligatorinae and Caimaninae.

Physical characteristics

A crocodile may be thought of as an elegant solution to the problem of catching prey, surviving unpredictable environments, conserving limited energy, and reproducing successfully. In appearance, crocodiles superficially resemble lizards, having scales, a long tail, and four limbs. But appearances can be deceptive, and a closer look reveals that crocodilians are unique.

All 23 species are broadly similar in appearance, varying mainly in size, scale patterns, color, and skull morphology. The smallest species is Cuvier's dwarf caiman (Paleosuchus palpebrosus); adult males rarely exceed 5 ft (1.6 m) in length and females 4 ft (1.2 m). Within the same family, the black caiman (Melanosuchus niger) and American alligator (Alligator mississippiensis) vie for largest size, yet rarely exceed 14 ft (4.3 m). Crocodylidae range from the diminutive dwarf crocodile (Osteolaemus tetraspis) at 6 ft (1.8 m) to the massive estuarine crocodile (Crocodylus porosus) that can exceed 16 ft (5 m). The

sole gavialid, the Indian gharial (Gavialis gangeticus) can also reach 16 ft (4.9 m). Females are always the smaller sex, and this is most apparent in estuarine crocodiles, where females of 10 ft (3 m) are considered to be very large.

As the largest living reptiles, males over 16 ft (4.9 m) may tip the scales at 1,100 lb (500 kg), but these are lightweights compared to rare individuals that exceed 18 ft (5.5 m) and 2,200 lb (1,000 kg). Although several species, including estuarine crocodiles and Indian gharials, are capable of attaining such sizes, evidence of these giants is scarce. The largest crocodile reliably measured and published in the literature, an estuarine crocodile from Papua New Guinea, was 20.7 ft (6.3 m) long. While unlikely to be the maximum possible size for this species, stories of even larger animals are difficult to verify. One fact is certain—crocodiles over 20 ft (6 m) are exceptionally rare.

Crocodilians undergo a dramatic increase in size from hatchling to adult. Over its lifetime, an estuarine crocodile may grow from a 12-in, 2.8-oz (30-cm, 80-g) hatchling to a 20-ft, 2,650-lb (600-cm, 1,200-kg) adult. A 20-fold increase in length and 15,000-fold increase in weight is quite a feat in the animal kingdom. Imagine, then, how this compares with the extinct Sarcosuchus, which reached 35 ft (10.7 m) and over 19,800 lb (9,000 kg)! Growth is most rapid when young, yet scientists are unsure whether adults reach a maximum size or continue to grow slowly until they die. The enormous sizes attained by extinct species such as Sarcosuchus and Deinosuchus may have been possible by maintaining those fast juvenile growth rates throughout a greater percentage of their lives.

Crocodilians are covered in a thick, leathery skin broken into various sizes and shapes of scales in particular areas. Scales on the back are large and rectangular, lying in parallel rows from shoulders to pelvis and continuing onto the tail. These dorsal "scutes" each contain a bony plate called an osteoderm ("skin bone") just below the surface. A tough covering of beta-keratin helps minimize water loss, although the more flexible alpha-keratin is found between the scales. Osteoderms not only offer protection, they are infused with blood vessels and function as solar panels, transporting heat from the surface to the body core during basking. Adjacent osteoderms are closely integrated like the beams of a bridge, providing support for the spinal column. Large nuchal plates protect the nape. Scales on the flanks and limbs are generally smaller, rounder, and softer to allow bending. Those on the belly are even, rectangular, and smooth to reduce friction sliding over the ground. Small osteoderms are found in the belly scales of most species. Thick, rectangular scales are present on the tail, with sharp, upward-pointing scutes providing extra surface area as the tail sweeps through water. Scales on the head are small, irregular in shape and thin, housing blood vessels and sensory nerves. Each species has a unique pattern of scales and osteoderms.

Deceptively, a layer of mud and dust often covers dry, basking adults, suggesting a bland coloration. However, most species exhibit distinctive color patterns, which enhance camouflage and aid communication. Dorsal color is typically tanned yellow to dark brown, overlaid with characteristic dark bands, spots, or speckles. Juveniles of all species are more vivid, their bright colors fading in adulthood. Ventral scales are creamy white with varying degrees of black pigmentation, except for the almost black bellies of dwarf caimans and dwarf crocodiles. Color mutations where pigment is usually absent are rare, genetic anomalies. Leucistic and albino crocodiles are as tempting to predators as their "white chocolate" appearance suggests, but they are popular tourist attractions in captivity, where they must be shielded from excess sunlight. Both short- and long-term changes in skin color have been

recorded in several species. Changes in mood, such as those caused by stress, and environmental temperature can dull skin color. Long-term change can be effected by the environment, with individuals from shaded areas becoming darker as black pigment (melanin) accumulates in the skin.

The crocodilian head always draws attention. The skull, although massive and sturdy, is infiltrated with air spaces. These spaces reduce weight without compromising strength, and provide extensive areas for muscle attachment and expansion. Two pairs of openings on either side of the cranium classify the skull as diapsid. There is considerable variation in skull and jaw morphology across all 23 species, and this has an ecological significance: broad jaws are reinforced by bony ridges to resist strong bite forces for crushing prey, while slender jaws slice with little resistance through water to seize slippery prey.

The head houses all the major sense organs, vital for navigation, communication, and hunting. Senses are concentrated on the dorsal surface, so they remain exposed even when the head is partially submerged. Remarkably, a crocodile can hide its entire body below the water while maintaining maximal sensory input from its surroundings. As masters of stealth and ambush, crocodiles have no equal.

The eyes of the crocodile are placed high on each side of the head, turrets that provide 270° of widescreen coverage plus 25° of binocular overlap directly ahead to accurately judge distance. The pupil, round and dilated at night to permit maximum light entry, is compressed to a thin vertical slit during daylight to protect the sensitive retina. Inside the eye, cone cells on the retina provide color acuity by day, and high densities of rod cells give excellent low-light sensitivity at night. These rods can change shape to further alter sensitivity. A layer behind the retina, the tapetum lucidum, is impregnated with guanine crystals to reflect light back across the visual cells. This effectively doubles visual sensitivity at night, and shining a beam of light directly into a crocodile's eye rewards the observer with a fiery red eyeshine. Visual cells are most concentrated in a horizontal band across the back of the retina, a fovea providing highest visual acuity where crocodiles need it most—along the same plane as water. To focus (accommodate), crocodilians change the shape of their lens using the ciliary body.

Three eyelids cover each eye. The upper lid contains bony ossification to protect the eye, large bony palpebrals in caimans lending "eyebrows" to their appearance. The lower lid lacks ossification and is responsible for closing the eye. The third eyelid, the nictitating membrane, sweeps laterally over the cornea to clean the eye and protect it from abrasion underwater. Although the nictitating membrane is transparent except for the ossified leading edge, crocodilians still see poorly through it. Lachrymal (tear) glands lubricate its passage via ducts connected to the nasal cavities. Fluids may even accumulate when the crocodile remains out of water—real "crocodile tears," yet an unlikely source for the popular myth.

The ears are located immediately behind the eyes, the eardrum protected by an elongated flap of skin. Hearing sensitivity can be altered by opening a slit in front of the flap, or lifting the flap upward. When submerged, the ears normally close, as hearing becomes secondary to the ability to feel vibrations through the water. Detectable frequencies range from below 10 Hz to over 10 kHz, and sound pressure levels below -60 dB can be detected within certain bandwidths. In other words, crocodilians have excellent hearing, on a par with birds and mammals. Peak sensitivities range from 100 Hz to 3 kHz depending on the species, which coincides with the bandwidth of calls produced by juveniles. Vocalization is well developed in crocodilians, with over 20 different call types from both juveniles and adults recognized.

Crocodilians can breathe when submerged by exposing the dorsal margin of their head and hence their raised nostrils. Inhaled air passes through sinuses separated from the mouth by a bony secondary palate, where any chemicals in the air are detected by sensory epithelial cells. The presence and direction to food is easily discerned, and smell plays an important role in chemical communication. In early crocodyliforms, the internal nostrils (choanae) opened in the front of the mouth, but over millions of years they moved back to the throat, a phenomenon termed post-nasal drift. The palatal valve, a fleshy extension of the tongue, completely seals the throat from the mouth, hence crocodilians breathe easily near the surface even if the mouth is flooded with water. The glottis, an opening to the trachea and lungs, is located directly beneath the choanae. By varying tension in muscles lining the opening, exhaled air is forced through a constriction capable of relatively complex vocal sounds. Amplification is provided by expanding the throat using the hyoid apparatus, a curved cartilage beneath the glottis. A curious bend in the trachea of several species may further amplify the sound, similar to the long, curved necks of cranes.

The tongue lies between each mandibular bone of the lower jaw, behind the mandibular symphesis (fusion). Hence in slender-snouted species with extended sympheses, the tongue is greatly reduced. Although relatively immobile, the tongue can be pushed against the roof of the mouth to manipulate objects or pulled down to create a pouch for hatchlings. Typically bright yellow or orange, the tongue's color may provide a social or warning signal when the jaws gape. Pores cover the surface of the tongue, through which "salt glands" produce a saline fluid in brackish or sea water in Crocodylidae and Gavialidae. Alligatorid pores play no role in salt secretion, supporting theories of a more recent marine dispersal phase for the Crocodylidae. Chemoreceptors lining the tongue detect chemicals in water, yet little is known of their sensitivity. Their importance is implied in their ability to detect food underwater, and in the role of pheromones secreted from chin and paracloacal musk glands.

High densities of dome pressure receptors (DPRs) cover scales on the head, particularly around the jaws. Disturbances of the water surface create pressure waves easily detected by DPRs, rapidly alerting the crocodile to potential prey near the head. Crocodilians also react rapidly to movement underwater (such as fishes) even when vision is unavailable. Similar pressure receptors, Integumentary Sense Organs (ISOs), are located on the caudal margin of body scales in Crocodylidae and Gavialidae, but not Alligatoridae. Their function is not fully understood, nor is the reason why alligatorids entirely lack them. However, evidence of DPRs exists in extinct crocodyliforms, suggesting their sensory role in water has long been part of their repertoire.

Betraying their terrestrial origins, crocodilians are surprisingly mobile predators on land. Although lacking the stamina for pursuit, their explosive force catches most prey unaware. Like all archosaurs, the hind limbs are significantly larger and stronger than the forelimbs, suited to the crocodilian propensity for launching the body forward at speed. Five toes are present on the front feet and four on the back, although residual bones from the fifth still exist. The inner three toes terminate with strong, blunt nails that provide traction; the outer one (back feet) or two (front feet) lack claws and bend backward during walking. There is extensive webbing between the toes on the back feet, but webbing is minimal or absent from the front feet.

The limbs are used to crawl, walk, and gallop. The crawl employs the limbs alternately to slide the body across mud, sand, or grass. When sufficiently motivated, the limbs can propel the body forward in a slithering manner at much greater speed, up to 6.2 mph (10 kph). In the uniquely crocodilian high walk, the feet rotate inward toward the body and support it from below. Lifting the head and belly clear of the ground enables the crocodile to traverse obstacles or rough terrain. In a few species, the front and hind limbs move in tandem to gallop. This springlike gait accelerates the crocodile up to 10.6 mph (17 kph) for several seconds until the safety of water can be reached. Cuban crocodiles (C. rhombifer) remind us of the frightening aggression of their terrestrial ancestors when they gallop toward a threat.

Water is clearly the crocodilian's preferred domain, a home for prey that live in the water and a magnet for prey that live on land. Mobility is possible through the powerful tail, which makes up half the body's total length. Flattened dorsoventrally to provide extensive surface area for propulsion, the tail is undulated laterally by powerful muscles. Limbs are swept back during rapid swimming, although when moving slowly they help the crocodile steer, brake, reverse, or walk across the bottom. So powerful is the tail that it can drive hundreds of pounds (or kilograms) of crocodile vertically out of the water to capture prey several feet (or meters) overhead.

Internally, the pleural cavity contains the lungs, and the visceral cavity houses major organs associated with digestion and reproduction. These cavities are separated by the bilobed liver and diaphragmaticus, a sheet of muscle analogous to the diaphragm in mammals. Inhalation is achieved by contracting the diaphragmaticus, which pulls the liver backward and expands the pleural cavity. Thoracic (intercostal) muscles also expand the chest, and reduced pressure in the lungs draws air in through open airways. To exhale, the diaphragmaticus and thoracic muscles relax, compressing the pleural cavity and forcing air out of the airways. Crocodilians control their buoyancy primarily through the volume of air in their lungs. By moving the liver, hind legs, and tail, subtle postural changes are also possible. When diving, air is forced out of the lungs and the crocodilian, which is considerably heavier than water, sinks rapidly. Swimming may facilitate this sinking, and by sweeping the hind legs forward the crocodilian can reverse and submerge simultaneously. Swimming or pushing off the bottom returns the crocodilian to the surface, and positive buoyancy is achieved by filling the lungs with air. Stones called gastroliths in the stomach typically comprise 1–5% of the crocodile's total weight, and their presence may provide additional ballast.

Situated between the lungs is the most complex heart in the animal kingdom, apparently the result of adaptation to

the demands of the crocodiles' semiaquatic lifestyle and their size. Unlike other reptiles, the crocodilian heart is fully divided into four chambers, as are the hearts of birds and mammals. Uniquely, valves under nervous and hormonal control can alter blood flow. These ensure that vital oxygenated blood circulates between essential areas during oxygen stress, such as while diving, while deoxygenated blood is sent to nonessential areas. During rest and normal exercise, blood in the right ventricle passes via a coglike valve to the pulmonary arteries and lungs to acquire oxygen. During diving, this valve constricts, and deoxygenated blood is diverted to the left aortic arch that leads to the nonessential visceral organs—a pulmonary-to-systemic shunt. Only a small volume is used to collect residual oxygen in the lungs. A second valve, the foramen of Panizza, connects the base of left and right aortic arches. The right aorta directs blood to the head, limbs and tail, and these vital areas require oxygenated blood during oxygen stress. The foramen of Panizza allows oxygenated blood to pass from right to left aortas (to visceral organs) only during rest and normal exercise, cutting them off when not needed.

Biochemical adaptations complement the action of the heart. Crocodilian blood contains complex hemoglobin molecules capable of carrying more oxygen molecules than those of any other vertebrate. Crocodilians also endure much higher levels of lactic acid (produced when oxygen is scarce) in their blood than any other vertebrate. Blood pH has been measured below 6.1 without serious consequences, a level that would kill any other vertebrate. The result? A submergence time of nearly two hours when quiescent, even longer under cool conditions. American alligators have remained trapped under ice for eight hours and survived. Heavy activity substantially reduces submergence time, but crocodilians need only to outlast their prey. The blood also houses complex antibacterial proteins capable of fighting off infection. Living in bacteria-filled waters, where injuries from fights are common, a strong immune system is essential. Crocodile blood has even been shown to kill "superbugs" for which scientists have no known cure.

Distribution

Crocodilians are found in over 90 countries and islands, generally in tropical and subtropical regions warm enough for successful reproduction. American and Chinese alligators, found in the highest latitudes of any species, do have a limited ability to survive seasonal freezing where deep water or shelter is available. Large adults can even endure being trapped in ice, as long as their internal organs do not freeze and their nostrils project above the surface.

Alligatoridae are restricted to North, Central, and South America, except for the Chinese alligator (A. sinensis), which occurs in eastern China. The stronghold of the Crocodylidae is Africa, India, and Asia, although a handful are found in the Americas. The single member of Gavialidae is found in India and adjacent countries. Estuarine crocodiles have the widest distribution (India to Vanuatu), although Nile crocodiles cover the greatest area (most of Africa and Madagascar). Spectacled caimans (Caiman crocodilus) number in the millions and are the most numerous throughout Central and South America. Introduced populations of certain species, particularly caimans, are established outside their natural ranges.

Crocodilians favor freshwater habitats, although several members of Crocodylidae tolerate higher salinity. Estuarine (also known as saltwater) crocodiles live in freshwater tidal rivers, hypersaline creeks, and along coastlines, and can travel at sea. Their ability to excrete excess salt through lingual salt

glands and produce concentrated urine make this possible. All species frequent freshwater and low-salinity areas where available, including tidal rivers, freshwater marshes, and both natural and artificial lakes and pools. Distribution is influenced by the density and diversity of prey, available nesting habitat, shelter for juveniles and adults, thermal conditions, seasonal changes, and competition between species. Temporary range extensions have occurred when competition from one species over another has been reduced due to hunting, etc.

Feeding ecology and diet

Crocodilians are renowned for their ability to acquire food, often violently. All species are carnivorous, and mostly generalist. A wide range of mammals, birds, reptiles, amphibians, crustaceans, mollusks, fishes, and insects are taken readily by adults of most species. There are various restrictions, however. Young juveniles are limited to small prey that enter or approach water, primarily insects, spiders, crustaceans, fishes, small reptiles, and amphibians. Juveniles eat regularly, each day if possible. As they grow, the size and range of available prey increases. Species with specialized foraging strategies as adults (such as gharials) begin to exhibit characteristic preferences.

Although anything that moves within striking range is often considered fair game for adult crocodilians, most species display some selection criteria. These may include prey availability, but also species-specific preferences influenced by morphology and ecology. Broad-snouted alligatorids with strong bites and blunt teeth include hard-shelled prey in their diet; slender-snouted species such as gharials have weaker bites, but their sharp, undifferentiated teeth and slender jaws are ideal for sweeping quickly through water to seize slippery fish. Many Crocodylidae possess jaws between these two extremes, reflecting a generalist diet influenced by prey distribution and seasonal availability. Species with more specialized jaws will, however, take other prey where available.

Crocodilians display several hunting techniques. Surprisingly, most prey are small and taken as they approach the head, even in very large adults. The kill zone is an arc traced by the head and neck, although some species literally dive onto prey just below the surface. Terrestrial prey are ambushed at the water's edge, the hunter is either submerged or exposes only the eyes and nostrils. Once within striking range, there is an explosion of teeth and water as the crocodilian propels itself forward using its tail and limbs. Larger prey are dragged into the water where they drown. Although not pack hunters, the presence of several crocodilians in the water speeds a prey's demise. However, capture is not always successful. Misses are common, and large prey bitten on the head, limbs, or body may escape, only to die later from their injuries.

Although there are stories of crocodiles using their tails to sweep prey off their feet, hard evidence is sorely lacking, though the tail is important in hunting. Larger crocodiles are often seen using the tail to herd small fish into shallow water to be scooped up with a sweep of open jaws. The tail can be used to push the body vertically out of the water, ideal for catching prey flying over the water or hanging in low branches. This behavior has been witnessed in many species. Several species are reported to form a living dam with their bodies, preventing migrating fish from escaping. By cooperating, many individuals increase their chances of success. Nile crocodiles frequently cooperate after large prey is captured, taking turns to hold the carcass while others spins their bodies to rip off mouthfuls of flesh. Crocodilians learn rapidly to associate events with outcomes, often attending predictable events such as prey migrations.

Once captured, small prey is deftly manipulated by the jaws for immediate swallowing; head raised, the prey is flicked into the throat under gravity. Larger prey is first crushed several times by the back teeth, perforating skin and shell to assist digestion. Prey too large to be swallowed is typically held firmly in the jaws, then the head is whipped violently to one side. This tears prey apart, and each piece is swallowed once retrieved. Very large prey is first dismembered by holding onto a piece with the jaws, then spinning the body axis several times to twist it off. The carcass is anchored by its own weight, or by other feeding crocodilians. Live prey are easily incapacitated by rolling, as defense against this maneuver is impossible. Once inside the stomach, food is subjected to highly acidic gastric juices. The action of the muscular stomach plus gastrolith stones slowly macerates flesh and renders bone and shell into smaller pieces. Only keratin (found in hair, nails, and turtle shell) is immune. Compacted balls of indigestible material are regularly coughed up.

Frequently classed as man-eaters, only a handful of species are considered a significant threat to humans. Most fatalities are reported from American alligators, estuarine crocodiles, and Nile crocodiles, the latter responsible for the greatest number of crocodile-related deaths each year with several hundred people estimated killed or seriously injured. Threats can be reduced significantly by educating people to the danger posed by crocodilians, and providing alternative means of accessing water.

Reproductive biology

The basic crocodilian breeding system is polygynous (one male, multiple females), although short-term monogamous pair bonding has been described in Nile crocodiles and possibly other species. Multiple paternity (several males, same female) has also been recorded in some social situations. Once sexual maturity is reached, dictated by size rather than age, reproductive activity follows an annual cycle. Environmental triggers such as changing temperature, rainfall, humidity, and day length trigger hormonal changes in each sex. In males, testosterone levels rise, testes increase in weight, and sperm production increases. In females, estradiol levels rise, triggering the liver to produce vitellogenin for yolk production in the ovaries, and follicle size increases prior to ovulation. Double clutches have been reported in mugger crocodiles (C. palustris) and Nile crocodiles, influenced by extended environmental conditions favorable to breeding.

As habitat and climate change geographically, the timing and duration of reproductive activities varies between species and even within a species' distribution. Courtship, mating, and nesting may occur over a period of several months (as in Nile and estuarine crocodiles), or may be concentrated into several weeks (as in American alligators). Johnstone's crocodiles, or Australian freshwater crocodiles (C. johnstonii), nest within a two to three week period, a phenomenon known as "pulse nesting."

Crocodilians exhibit two nesting strategies: hole nesting and mound nesting. In the former the female selects a soft substrate, such as sand or mulch, and excavates a chamber several inches deep using her hind legs. After laying her eggs, the chamber is concealed again. In mound-nesting species, the female first scrapes material, such as vegetation, soil, or mud, into a mound using her front and hind legs. She also rips up fresh vegetation with her jaws. The resulting mound can be over 3.3 ft (1 m) high and 6.6–9.8 ft (2–3 m) in diameter. Once the mound is complete, the female behaves like a hole nester: she excavates a chamber into the top of the mound with her hind legs, lays her eggs, conceals them, and compacts the nest using her hind legs and body. Only Crocodylidae and Gavialidae excavate hole nests, in those species that nest during the dry season or when little vegetative matter is available. Mound nests are built by Alligatoridae and some Crocodylidae, typically nesting during the wet season or in areas that inundate easily, as the additional height reduces the risk of eggs being drowned by floods. American and Cuban crocodiles have been reported to choose either hole or mound nests, depending on climate and habitat.

Nesting location may be determined by available materials, proximity of water, temperature, and even social factors. Females of more territorial species choose solitary nesting sites, isolated visually or by distance from those of other females. Favorite sites may be reused each year, although not necessarily by the same female. More gregarious species may use communal sites. Although under the vigilant watch of several females, there are disadvantages to communal sites. Late nesters may inadvertently dig up older eggs, and predators have an easier time finding eggs where nests are concentrated. Frequency of nesting is also under social pressure. In the wild, between 10% and 80% of females of a given species may nest each year; the percentage determined by the amount of nesting habitat available, the territorial nature of the females, and species-specific differences.

As with porcupines, people are curious how crocodilians manage to mate without causing each other grief! In reality, it is a gentle affair (once the competition has been dispensed with, that is). To copulate successfully, males must court females to gain their consent. Males of some species, such as estuarine crocodiles, establish territories that contain a number of females, others, such as American alligators, display competitively to attract females. Courtship may be elaborate or subtle, involving mutual signaling on a visual, olfactory, auditory, and tactile level. Alligators combine rumbling bellows with infrasonic vibrations, the water dancing across their backs proving a potent aphrodisiac for females. Gular musk glands are rubbed across the head and neck in mutual appeasement, and several minutes of head- and tail-raising postures are necessary for consent. Once she consents, the female allows the male to press her underwater. To align his vent with hers, the male rolls the female's body in one direction while rotating his tail in the other, using limbs for purchase. Male crocodilians have a single penis, unlike the hemipenes of most other reptiles. Copulation can last several minutes, and may be repeated over a period of days, although most males attempt copulation with as many females as possible. In captivity, males have been reported copulating with almost 20 females. Copulation may take place in shallow or deep water.

After fertilization, eggs are retained in the oviduct for two to four weeks, although periods of six months have been reported in some spectacled caimans. Embryos grow to around 20 somites (cells) before laying, with development believed to resume once eggs are exposed to air. Freshly laid eggs are covered in a fraction of an inch (several millimeters) of mucus, which cushions their impact as they slide into position. Mucus may also prevent gas exchange and hence further development until laying is complete and the mucus dissolves. Clutch size varies greatly: larger species lay up to 70 eggs, smaller ones as few as 10. It can take between 20 and 90 minutes to lay the entire clutch, during which time the female becomes curiously docile. Each egg contains the yolk (nutrient storage), albumen (water supply), leathery inner shell membrane, and hard, calcified outer shell membrane (protection, control of water and gas exchange). The embryo, lying atop the yolk, attaches to the inner shell membrane 24 hours after laying. As development continues, an opaque white band spreads around the egg's axis before eventually encompassing the entire egg.

Several important variables influence embryo development. Nest temperatures may fluctuate between 84.2°F (29°C) and 93.2°F (34°C), but small changes have significant effects. On average, incubation time lasts 70–90 days, yet higher temperatures reduce this and lower ones increase it. Temperature also determines sex. The phenomenon of temperature-dependent sex determination (TSD) is found in crocodilians, marine turtles, and some lizards. Unlike genetic sex determination (GSD), the sex of the embryo is determined not by sex chromosomes at fertilization, but by a critical temperature-sensitive period during incubation (the middle third). In all crocodilians, the greatest percentage of males is produced around 87.8–89.6°F (31–32°C), with more females produced above and below this temperature. Temperatures above 93.2°F (34°C) and below 84.2°F (29°C) produce almost 100% females, although females produced at higher temperatures suffer higher mortality and genetic deformities. Above 95°F (35°C) and below 80.6°F (27°C) embryos rarely survive. The size of hatchlings, their growth rate, and even preferred basking temperatures are influenced by incubation temperature.

All species nest during warm seasonal climates, providing appropriate ambient temperatures for incubation. Solar radiation provides additional heat, although many nests are built in the shade to reduce overheating, and nesting substrate buffers the eggs from extreme temperature fluctuations each day. Mound nests generate heat from the breakdown of plant materials, and even the developing embryos provide some metabolic heat during the later stages of incubation. The smooth-fronted caiman (Paleosuchus trigonatus) typically nests in closed-canopy forests, where ambient temperatures may be insufficient for optimal egg development. To address this, caimans build nests within or adjacent to termite mounds—metabolic heat produced by the termites helps to warm the nest. The female's presence is often required to break open the nest and free the hatchlings. Rainfall helps to cool nests, and some females have been observed urinating on the nest. As a suggested cooling mechanism the volume involved may be insufficient, but it may play a role in chemical marking as hatchlings recognize chemicals in contact with their eggs.

Pores permeating inner and outer shell membranes allow gas exchange, and both high humidity and oxygen are necessary for development. Embryo demands increase further as development continues. Development seems highly susceptible to perturbation, yet crocodilian nests provide an effective environment for incubation. But not always. Exposed nests can overheat, and those built in areas prone to flooding are easily submerged. More than 12 hours underwater, particularly later in development when oxygen demands are higher, can spell disaster. Another threat faces developing eggs—nest predators such as monitor lizards, wild pigs, raccoons, even ants. Females of most species defend the nest, often fasting for over two months to remain vigilant, but predators can still catch her off guard.

Eventually the demands of the embryo exceed the capability of the egg and hatching occurs. Shortly before emergence, the fully developed embryos may vocalize. Calls propagate from one egg to the next, producing a chorus audible to the adult from 165 ft (50 m) away. The female is typically much closer to the nest, often observed resting her throat directly above the nest chamber close to hatching. The female scrapes back sand, mud, or vegetation from above the eggs with her front legs, and the vibration stimulates the eggs to hatch. Some hatchlings head for water, but others remain and vocalize, often with head raised to encourage the female to carry them in her jaws. By lowering the tongue, a gular pouch is created to hold hatchlings. Some species transport hatchlings one at a time, others, such as Nile crocodiles, transport several. The female carries them to water, opens her mouth, and washes the hatchlings out with a sweeping motion of the head before returning to the nest. Hatchlings form small pods or crèches, hiding amongst shoreline vegetation. Not all species perform hatchling transport, and puncture marks caused inadvertently by sharp-toothed females may indicate why not. Infertile or dead eggs are normally eaten by the female, which led to early speculation that females ate their young! In captivity, territorial males of certain species have been observed assisting the female to open nests, hatch eggs, and transport hatchlings. Wild Nile crocodile males occasionally guard juveniles after hatching, but male parental care is atypical.

Female protection of juveniles after hatching may last for days (as in Johnstone's crocodiles), weeks (as in Nile crocodiles), or even up to two years (as in American alligators). Hatchlings remain in close proximity to the female, often using her as a convenient basking platform. Vocalization is well developed in crocodilians, and is an important component of juvenile life. Contact calls maintain group cohesion and alert siblings to the presence of food. Distress calls scatter individuals and bring the adult female aggressively to bear. The level of parental care in crocodilians is fascinating. In spectacled caimans, pods from different females may combine into larger crèches tended by resident adults. Even more remarkable, adult females of three species (broad-snouted caimans, Orinoco, and Siamese crocodiles) have been observed feeding juveniles. The female macerates the carcass and juveniles tear off small pieces. This level of parental care is unprecedented for reptiles, and perhaps reminds us of the closer taxonomic affinities between crocodilians and birds.

Conservation status

Four of the 23 crocodilian species (Chinese alligator, Orinoco crocodile, Philippine crocodile, Siamese crocodile) are considered Critically Endangered, with a further three (Cuban crocodile, false gharial, Indian gharial) listed as Endangered and considered at risk of extinction. In what is considered the most dramatic recovery of any large vertebrae group, 16 of the 23 species went from Endangered to abundant or not threatened in the last 30 years of the twentieth century. These species' previous decline was attributed primarily to overhunting (for skins) and habitat loss. Recovery was due to a combination of species protection, habitat protection, suppression of illegal trade, and enlightened management programs promoting sustainable use of wild populations as an incentive for their conservation. Efforts to improve the status of the 7 remaining endangered species continue as of 2003.

Resources

Books

Alderton, D. Crocodiles and Alligators of the World. New York: Facts on File, 1991.

Behler, J. L., and D. A. Behler. Alligators and Crocodiles. Stillwater, MN: Voyager Press, 1998.

Campbell, G., and A. L. Winterbotham. Jaws Too: The Natural History of Crocodilians with Emphasis on Sanibel Island's Alligators. Ft. Myers, FL: Sutherland Publishing, 1985.

Grigg, G., F. Seebacher, and C. E. Franklin. Crocodilian Biology and Evolution. Sydney: Surrey Beatty and Sons, 2001.

Guggisberg, C. A. W. Crocodiles: Their Natural History, Folklore, and Conservation. Harrisburg, PA: Stackpole Books, 1972.

McIlhenny, E. A. The Alligator's Life History. Boston: Christopher Publishing, 1935.

Minton, S. A., Jr., and M. R. Minton. Giant Reptiles. New York: Scribner, 1973.

Neill, W. T. The Last of the Ruling Reptiles. New York: Columbia University Press, 1971.

Richardson, K., G. J. W. Webb, and S. C. Manolis. Crocodiles: Inside Out. A Guide to the Functional Morphology of Crocodilians. Sydney: Surrey Beatty and Sons, 2002.

Ross, C. Crocodiles and Alligators. New York: Facts on File, 1989.

Webb, G. J. W., and S. C. Manolis. Crocodiles of Australia. Sydney: Surrey Beatty and Sons, 1989.

Organizations

Crocodile Specialist Group, Florida Museum of Natural History. Box 117800, Gainesville, FL 32611-7800 USA. Phone: (352) 392-1721. Fax: (352) 392-9367. E-mail: prosscsg@flmnh.ufl.edu Web site: <http://www.flmnh.ufl.edu/natsci/herpetology/crocs.htm>

Other

Bibliography of Crocodilian Biology. January 18, 1996 [cited January 2003]. <http://utweb.ut.edu/faculty/mmeers/bcb/index.html>

Crocodilians: Natural History and Conservation. December 2002 [cited January 2003]. <http://www.crocodilian.com>

Adam R. C. Britton, PhD