Artiodactyla

(Even-toed ungulates)

Class Mammalia

Order Artiodactyla

Number of families 10

Number of genera, species 82–84 genera; 221–227 species

Introduction

Artiodactyls are one of the two living orders of terrestrial mammals that comprise the ungulates, or hoofed mammals. These orders are distinguished primarily by the animals' feet: the Artiodactyla are known as the even-toed ungulates in contrast to the Perissodactyla, or odd-toed ungulates. The name Artiodactyla comes from the Greek words artios, meaning entire or even numbered, and dactylos for finger or toe. Artiodactyls are a highly successful order and the most abundant large land mammals living today with more than 220 species worldwide. This order includes many familiar wild species such as antelopes, deer, bison, and giraffes, along with the familiar and important domestic species such as camels, cattle, goats, pigs, sheep, and water buffalo.

Although many artiodactyl species are relatively large and well known, scientists are still discovering new species. Since 1992, five new species of artiodactyls have been described, including one (Pseudoryx), and possibly another (Megamuntiacus), making two new genera. Each of the new species occurs in Southeast Asia (Laos, Cambodia, Vietnam). In addition, the Vietnam warty pig (Sus bucculentus) previously thought to have become extinct, was rediscovered, and there was also a new species of Bovidae discovered based on horns of the supposed "Linh Duong" (Pseudonovibos spiralis), although this may be a hoax as the horns of at least some specimens have turned out to be fashioned from domestic cattle horns.

Evolution and systematics

Understanding the evolutionary beginnings of the early artiodactyls, like that of the early ungulates, is hampered by an incomplete fossil record. Also, the artiodactyls appeared abruptly, along with early perissodactyls, without any clear intermediate forms between the early ungulates and the early artiodactyls. Some aspects of the evolutionary story are difficult to follow because the characteristics used to assign taxonomic position do not fossilize. For example, modern artiodactyls are divided into three suborders—non-ruminants, tylopods, and ruminants—based on the morphology of their digestive tracts, soft internal structures that are not preserved in fossils.

The oldest known fossils, clearly referable to artiodactyls, are in early Eocene deposits from Holarctica (Asia, Europe, and North America). These earliest artiodactyls were relatively abundant and widespread, and include Diacodexis and related genera in the Dichobunidae or Diacodexeidae. All were small mammals about the size of a rabbit or hare, weighing probably less than 11 lb (5 kg). They are considered to be early artiodactyls because they had a double-pulley astragalus (part of the ankle joint), which is a defining characteristic of this order, as well as other limb adaptations such as increased length for cursorial locomotion. However, the teeth of Diacodexis were still bunodont (low-crowned with rounded cusps), suggesting omnivorous food habits, and the skull shows no other traits diagnostic of artiodactyls. The sudden and widespread appearance of the early artiodactyls at the beginning of the Eocene about 55 million years ago (mya) suggests that they might have evolved elsewhere other than Holarctica. Perhaps they arose in Africa, India, or Central or South America and entered the northern continents only when physical or climatic barriers disappeared.

What is even less certain are the ancestors of these early artiodactyls from amongst the known fossil condylarths. So far, the closest condylarths to Diacodexis are the raccoon-like arctocyonids of the middle Paleocene. They were also small, being probably no more than 11 lb (5 kg) with long tails and teeth, suggesting an omnivorous diet. There is a tentatively

identified arctocyonid similar to Chriacus, a primitive oxyclaenid condylarth from the Paleocene, as being closest to the oldest artiodactyls so far discovered.

The family Dichobunidae, to which Diacodexis probably belonged, is the most primitive group of artiodactyls discovered so far. They are placed in the suborder Paleodonta, along with the closely related Leptochoeridae and the Entelodontidae. The entelodontids were much more advanced than either of the other two families and resembled giant pigs. In one genus, Archaeotherium, their elongated skulls had characteristic processes protruding from the jugal bone, as well as bony knobs on the lower jaw, reminiscent of the modern African warthog (Phacochoerus africanus). The incisors were blunt and heavy, while the canines were robust and capable of inflicting serious injury. The small molars were almost pig-like and, along with the premolars, were well spaced along the jaw. Their limbs had between two and three digits, with separate metapodials, although the ulna and radius were fused. Paleodonts have been found mainly in Europe, but also North America. They appeared in the early Eocene and became extinct by the end of the Miocene.

The suborder Ancodonta, another group of primitive, presumably non-ruminant artiodactyls, includes a rather loose grouping of three families: Anoplotheriidae, Anthracotheriidae, and Caenotheriidae. The anoplotheres were medium-sized ungulates that became extinct in the Oligocene. Anthracotheres, which probably evolved in the Eocene and flourished in the Oligocene, began as dog-sized mammals that evolved to hipposize and are thought to have eaten soft plants and lived a semiaquatic life in swamps. Their remains have been found in Africa, Asia, Europe, and North America, and representatives of this family lasted until the Pleistocene. In the early Miocene (about 18 mya), they are believed to have led to the modern hippopotamuses. The caenotheres were small, four-toed ungulates ranging in size from rabbits to small antelope that became extinct in the Miocene. Although no representatives of these three families exist today, genetic evidence supports the idea that hippos did not descend from the Old World representatives of Tyassuidae as previously suspected. They are more likely to have originated from within the suborder Ancodonta and, based on morphological characteristics, thought to have evolved from the anthracotheres.

Two families, the Agriochoeridae and Merycoidodontidae, are grouped together in the suborder Oreodontae. Their remains have been found only in deposits from Central and North America. The Merycoidodontidae were a very diverse group of small-and medium-sized, stocky-built herbivores, the largest of which was said to be about the size of a wild boar. They were highly successful having appeared in the late Eocene, flourished in Oligocene and Miocene, before becoming extinct in the Pliocene. Early forms had four prominent toes on the fore and hind feet, with a small almost vestigial fifth toe on the fore feet; in later forms, this fifth toe was lost. Their teeth showed interesting and characteristic modifications. There was no diastema (gap), but the lower canines had become incisor-like, while the first premolars had replaced the lower canine in form and function. In most forms, the orbit was closed and the skull often relatively large compared to the rest of the body so that they resembled modern peccaries in many ways. At least two forms showed skull characteristics suggestive of a proboscis. Most members of this family were plains-dwellers, but some were thought to have had an aquatic lifestyle similar to modern hippos. This is based on their skulls in which the eyes and nostrils are located high on the skull, similar to aquatic species. The Agriochoeridae, while less successful, are an equally interesting group of early oreodontid artiodactyls. They shared the same modifications of the lower canines and first premolars, but had a diastema after the upper canine and lower canine-like (caniniform) first premolars. Unlike the merycoidodontids, these animals had an open orbit and a defined saggital crest. Their lumbar region suggested an animal that could leap like a cat, and they also had a long heavy tail. They had five toes, although the first digit was much reduced, and rather than hooves, the toes terminated in claws. Despite this resemblance to carnivores, the teeth suggested that they were herbivorous. They also appeared in the late Eocene, but became extinct at the end of the Oligocene.

Toward the end of the Eocene, the world's climate began to change and by the beginning of the Oligocene epoch 38 mya, the Northern and Southern Hemispheres experienced definite seasons. Seasonality of climate resulted in significant and predictable variation in the growth and abundance of plants. Under these new conditions, both plants and the herbivores feeding on them evolved rapidly. Artiodactyls especially began to diversify and many large species evolved, with all but the pigs and peccaries becoming obligate herbivores. Molars of herbivorous artiodactyls evolved selenodont (crescent-shaped) enamel patterns adapted to grind plant food into small particles, to be followed much later in the Miocene by hypsodont (high-crowned) cheek teeth when the grasslands became established as an important terrestrial ecosystem.

When grasses first flourished about 20 mya in the Miocene, open savannas became a widespread ecosystem and the first specialized grazing ungulates began to appear. Browsing was not abandoned, but many species had mixed grazer-browser habits. Large pecoran ruminants, having either horns or antlers on their skulls, appeared in the early Miocene. These included cervids, bovids, giraffids, and the okapi-like palaeomerycids. By the end of the Miocene, all modern artiodactyl families were present.

In the mid Eocene, helohyids such as Helohyus appeared. These were primitive artiodactyls, somewhat larger than Diacodexis and with more robust limbs. These probably gave rise to the primitive pig-like Propalaeochoerus, which appeared in the late Eocene. By the beginning of the Oligocene, about 40 mya, the pig-like mammals had split into two families, the true Old World pigs (Suidae) and the New World peccaries (Tayassuidae). Both these modern groups have bunodont, relatively low-crowned molars, although in some ancestral forms, the molars are referred to as bunoselenodont because they show similar features to the crescent-shaped molars typical of ruminants. The earliest known peccary is Perchoerus, while the first recognized true pig is Paleochoerus. The ancestor of the modern Sus is probably Hyotherium from the early Miocene, which exhibited an elongated skull and tusks oriented laterally.

The earliest primitive tylopod was probably the small, four-toed Poebrodon of the late Eocene, followed in the mid Oligocene by Poebrotherium, a taller, longer-necked species with fused metapodials and each foot reduced to two toes. Subsequently, evolution in the camels saw the pads replacing hooves and a digitigrade rather than unguligrade posture. Miocene fossil footprints indicate that they had also developed a pacing rather than trotting gait. Miocene camels included Protomeryx in the early Miocene and Procamelus later in this epoch. Lama appeared to have split off at this time, but the other camels continued with the Pliocene (Pliauchenia) and then modern camels (Camelus) appeared in the late Pliocene. Camels probably originated in North America before dispersing to South America and Eurasia in the late Pliocene.

The late-Eocene Hypertragulidae showed signs of selenodont enamel and higher-crowned cheek teeth and so were probably primitive ruminants. Their upper incisors were reduced in size and, while the upper canine was little changed, the lower canine was reduced and incisiform (incisor-like). Although they had only four toes on the hind feet, they still retained five on the front, but the lateral toes were reduced in size. Their limbs were elongated, which together with their foot structure suggested they were able to run fast. The tragulids proper appeared in the Oligocene, showing a further reduction in the number of toes to four, with reduced lateral digits on both front and hind feet. The most advanced ruminants appeared sometime in the late Eocene–early Oligocene.

They had further modifications of the foot bones, and more complex cheek teeth.

One group of these early ruminants gave rise to the Giraffidae, Bovidae, Moschidae, Antilocapridae, and Cervidae. Eumeryx was a deer-like animal that appeared in the Oligocene and probably gave rise to the earliest giraffes and deer. At the beginning of the Miocene, two early giraffids appeared, Climacoceras and Canthumeryx, followed shortly after by Paleomeryx and Palaeotragus. The latter was short-necked, but possessed bony projections from the skull similar to the horn structures of modern giraffes. In the late Miocene, Samotherium, another short-necked giraffid appeared, after which the first members of the genus Okapia were recognized. It was not until the Pliocene that the long-necked giraffids (Giraffa) were seen.

Bovids first appeared in the fossil record in the late Oligocene, however, they were represented only by teeth typical of this family. The first, more complete representative of the early bovids was Eotragus from the middle Miocene. It was perhaps similar in size and habits to modern duikers (Cephalophinae), with small horns and slender limbs. Following Eotragus, the Tragocerinae evolved later in the Miocene. This was a primitive bovid group with a variety of horn shapes. The closest modern forms to these are probably the chousinga (Tetracerus quadricornis) and the nilgai (Boselaphus tragocamelus), both from India. The earliest sheep (Oioceros) and gazelles (Gazella) made their appearance in the mid to late Miocene about 14 mya. Pachyporlax, another genus from the late Miocene and a relative of the nilgai, is thought to be related to the earliest wild cattle such as Leptobos and Parabos, which appeared in the early Pliocene.

Some authors suggest that pronghorns (Antilocapridae) should be included within the Bovidae, but analysis of nuclear DNA suggests that they are a unique lineage. The antilocaprids arose from the Merycodontinae in North America, with the earliest form, Paracosoryx prodromus, being recognized from the early Miocene, about 20 mya. The Antilocaprinae followed in the late Miocene and appear to

have replaced the smaller Merycodontinae. The antilocaprins evolved into a highly successful and diversified group, especially in the Pliocene, and persisted until the Pleistocene, after which only one species remained, the living American pronghorn (Antilocapra americana). The antilocaprids are considered to be most closely related to the cervids rather than the bovids, as was previously thought. Hence, they have been placed together with the Cervidae into the Cervoidea. The deer-like Eumeryx of the Oligocene was followed in the early Miocene by Dicrocerus. This was the first true cervid to possess antlers, but they were short simple antlers and resembled those of modern-day muntjacs. Diversification of the Cervidae occurred later in the Miocene and also in the Pliocene.

By the late Pliocene, the Artiodactyla assumed more modern forms, and included many of the groups living today. The living mouse deer, or chevrotains (family Tragulidae), are the most primitive of the true ruminants. They are thought to have changed very little and, in fact, still resemble the early ancestors of this group. Analysis of nuclear DNA suggest that the Cervidae and Bovidae appear to be sister taxa, and the Giraffidae more primitive. The Antilocapridae are probably most closely related to the Cervidae and are placed together with the Moschidae in the Cervoidea.

Based on morphological considerations, the accepted taxonomy of modern artiodactyls recognizes three suborders: Suiformes (pigs, peccaries, and hippopotamuses), Tylopoda (camels), and Ruminantia (true ruminants). However, this may soon change. Cetaceans have always been considered closely related to ancestral artiodactyls based on fossil material, but until recently the link was not clear. Whales were considered to have arisen from within the mesonychids, a member of the Condylarthra, which are considered derived from arctocyonids. A key feature used to identify artiodactyls in the fossil record is their double-pulley astragalus. In the year 2000, two fossil early whales were discovered in 47-million-year-old Eocene deposits from Pakistan. One of these whales, Artiocetus clavis, possessed such an astragalus. This find, together with genetic evidence from other studies, suggests a clear evolutionary link between cetaceans and artiodactyls. In fact, some scientists contend that the name Artiodactyla should be replaced with Cetartiodactyla to indicate that whales belong to the same order. Based on the evidence to date, the closest ancestor of the cetaceans is believed to be a forerunner of the modern hippo, a notion that is not accepted by those who consider that there is strong fossil evidence showing whales are derived from the mesonychids. If the order Cetartiodactyla is accepted, it would be comprised of five rather than three modern suborders: the monophylic Suiformes (pigs and peccaries), the hippos in the Ancodonta, the Cetacea, Tylopoda, and Ruminantia.

Since the order Cetartiodactyle is not yet accepted, the Artiodactyla is considered to be divided into three suborders with 10 families. The suborder Suina contains three families: the Suidae (pigs), Tayassuidae (peccaries and javelinas), and Hippopotamidae (hippopotamuses). The Tylopoda contains only the family Camelidae (camels and llamas), while the sub-order Ruminantia is comprised of the Tragulidae (mouse deer and chevrotains), Giraffidae (giraffe and okapi), Cervidae (deer), Antilocapridae (pronghorn), and Bovidae (antelopes, cattle, sheep, and goats). The modern Artiodactyla include a total of 79–81 genera and 217–223 species. A meaningful number of subspecies is difficult because many are disputed, but there are probably more than 800 recognized.

Physical characteristics

Artiodactyls vary greatly in physical characteristics. They range in size from the diminutive mouse deer (Tragulidae) of Southeast Asia, some of which weigh less than 2 lb (1 kg) and stand no more than 14 in (35 cm) at the shoulder, to the common hippopotamus (Hippopotamus amphibius) weighing almost 10,000 lb (up to 4,500 kg). The head varies in shape from a short to long facial structure, with hairy to naked muzzle that is either large or small. The laterally positioned eyes are often large with long lashes, and the ears, with either rounded or pointed tops, can be relatively large or small compared to the head. Neck length can be short to very long. In most species the hair covering the neck is relatively short, but some species, especially adult males, have longer hairs along the ventral edge forming a clearly defined ruff. In others, a flap of skin, or dewlap, hangs from the ventral surface. The back may be straight, or the shoulders higher than the rump as in bison and gaur, or the reverse as seen in the duikers. Tail length also varies widely, from very short to long. Hair length may be long over the entire tail or long only in a terminal tuft. The legs can be relatively long to short and relatively slender in most species, except in hippos, whose legs are quite stout. Hooves also vary from narrow to broad in width and short or long in length. The body pelage, made up of longer guard hairs and shorter underfur, shows a range from short and smooth to dense and long, although the longer hairs are present usually only in certain body regions. The longest guard hairs of any mammal are found on the musk oxen of the Arctic. Hair coat usually changes with the seasons, and in some species, coloration differs between sexes and among age classes.

The skull lacks an alisphenoid canal, and there is no posterior expansion of the nasal bones. The teeth are heterodont and highly specialized according to food habits, with most being adapted for a wholly herbivorous diet. The bovids, cervids, and giraffids have all lost the upper incisors. The lower canines are usually small and modified to function as incisors (incisiform). The upper canines in bovids and giraffids are absent. They are also absent in most cervids, but in some species in this family, they are present though small and blunt (e.g., Cervus). In the Tragulidae, muntjacs, and some of the small antlerless deer, upper canines are enlarged, while in the Suidae, Tayassuidae, Hippopotamidae, and Camelidae both upper and lower canines are well developed. There is almost always a space, or diastema, on the lower jaw, between the

canine and first premolar. The dental formulae vary: (I0–3/3, C0–1/1, P2–4/2–4, M3/3) × 2 = 30–44.

Female artiodactyls have two to four teats, except Suidae, which have six to 12. The gestation period lasts from five to 11 months, depending on species. Triplets are rare, except in suids. Physiological sexual maturity is typically reached at 18 months of age in both sexes, with females generally giving birth for the first time when they are two years old, In many species, males only begin to fully participate in mating several years later than females. Longevity varies considerably with species, ranging from 10–30 years, but average age at death (life expectancy) is much lower.

The defining characteristics of the Artiodactyla are their number of toes (digits) and the structure of their astragalus. Almost all have fewer toes than the five of the ancestral vertebrate plan. Except for two species (Pecari and Tayassu) in the Tayassuidae, for which there is conflicting evidence about the number of toes on the hind feet, all other artiodactyls have an even number of functional toes, either two or four, on each

foot. The first digit of the original mammalian plan of five digits has been lost during the evolution of artiodactyls. As a result, the symmetry of the artiodactyl foot passes between the middle two digits (third and fourth), creating a limb structure referred to as paraxonic, in which the weight is born on these two central elements. In artiodactyls with two main toes, the second and fifth digits are either reduced, vestigial, or absent; when present, they are referred to as lateral hooves or dew claws. The terminal phalanges of the two weight-bearing toes and the dewclaws are covered with keratin sheaths called hooves. In species with four functional (weight-bearing) toes, the toes form a spreading foot. Usually there are no hooves, but the nails at the end of the four toes are often enlarged. Most artiodactyls also have elongated metapodials that, except in pigs, are fused into a single functional unit.

Most artiodactyls share the same adaptations for speed as do other ungulates, including lighter structured feet and limbs, reduced lower limb musculature, strong attachment of the hind limbs and loose attachment of the front limbs to the vertebral column, and leg movements restricted to a fore-aft motion. Artiodactyls have another adaptation that affects limb movements and increases running efficiency. The astragalus, a tarsal (ankle) bone in their hind limb, has deeply arched grooves on both ends where it articulates with the corresponding limb bones. These grooved joints help resist lateral motion, and also create an efficient double-pulley system that increases the flexibility and springiness of the lower hind limb.

Generally, the hard hooves, coupled with small feet and long, light limbs, provide excellent adaptations for fast running. However, some species of artiodactyls show secondary foot adaptations to travelling over soft ground. In dromedary (Camelus dromedarius) and Bactrian (C. bactrianus) camels, for example, both toes on each foot are enlarged relative to the body size, thus providing a greater surface area that helps prevent the animal from sinking deeply into loose sand. Similarly, caribou and reindeer, which travel long distances over snow in winter, have relatively large main and lateral hooves. Together, these four toes serve to increase the foot's surface area, and in effect act as snowshoes to help the animals negotiate areas of deep snow. These deer also use their large feet to paw through the snow and uncover buried lichens.

Almost all species of artiodactyls have weapons of some kind, depending on family; for example, unbranched horns are present in all Bovidae and Giraffidae, forked horns in Antilocapridae, antlers in the Cervidae, and well-developed canines or tusks are typical of the Suidae, Tayassudiae, Tragulidae, and Moschinae. Well-developed upper canines are also found in some species of deer such as the antlerless water deer (Hydropotes), while the small-antlered muntjacs (Muntiacus) and tufted deer (Elaphodus cephalophus) have both antlers and large upper canines. New antlers grow each year and are shed, usually soon after the rut (mating season). In the bovids such as argali (Ovis ammon), horns are not shed but continue to grow throughout the animal's life. However, in the pronghorn (Antilocapra americana), which also possesses horns similar in structure to bovids, the keratinized horn sheath is shed each year.

In almost all cases, these weapons are largest in adult males and are either smaller or absent in females. Horns, antlers, and tusks are used primarily for intraspecific competition and not for defense against predators, as was first pointed out by Charles Darwin. He argued that the great variety of weapons, most of which were not particularly effective against predators, along with the fact that females either lacked or had much smaller weapons than males, and that males rarely defended females and young, supported an intra-rather than inter-specific function for these weapons. It is true, however, that under extreme circumstances, an animal might use its weapons against a predator, but this is usually a last resort and is not their primary function.

The coat or pelage consists of two parts: longer, stout guard hairs and shorter, usually finer, underfur. The guard hairs serve to shed rain and snow, and together with the underfur help control heat exchange. Most breeds of domestic sheep (Ovis aries) have been selectively bred so that they no longer have guard hairs, but have retained the underfur, or wool. Pelage color varies greatly across species, ranging from white to black, but most often varying shades of brown. The coat coloration of young artiodactyls in the first few months of life often is often distinctly different from the adults, and in some species, male coat color is related to age and social status. Species living in temperate and arctic regions shed their warm winter coat in early spring and grow a sleeker, shorter one for summer. Many species have a distinct color pattern. White spots or stripes against a dark coat can break up the animals outline, making it more difficult to see in the dappled sunlight filtering through forest vegetation. Other conspicuous coat patterns are used in social communication; for example, the erection of the hairs on a white rump patch signals danger to other members of the group.

Many species of artiodactyls have glands in different areas of the body, that they use for communication. Most are epithelial (skin) glands and are often paired, one on each side of the body. They secrete odoriferous chemical secretions either as volatile chemicals or waxy substances. Many territorial species use glandular secretions, sometimes along with urine and feces, to mark territorial boundaries. For example, adult male Thomson's gazelles (Gazella thomsonii) deposit secretions from their preorbital glands on twigs and tall grass stems along territorial boundaries. Some non-territorial species also use glandular secretions to mark objects in their environment, perhaps to advertise their presence. For example, male deer commonly rub their antlers against shrubs or small flexible trees, so species with glands on their heads probably leave olfactory signs, along with visual evidence of the scratched and broken vegetation. Muntjac use their large preorbital glands located in front of their eyes to mark conspecifics. Other species use their glands for self-marking, for communicating alarm, and possibly to advertise their physiological condition. Urination accompanied by wallowing is a common example of self-marking used by male artiodactyls in the mating season to advertise their presence. Other forms of self-marking include hock-rubbing, seen in some species of odocoilid deer, and urination spraying shown by caprid species such as alpine ibex (Capra ibex). Again, males in the rut most frequently perform these behaviors. Alarm signals may be given when the tail is raised in alarm, or from the tarsal glands when the hairs of the gland are erected on the hind legs. Interdigital or pedal glands found between the main hooves of many artiodactyls are thought to mark trails and bedding sites. In general, however, the role of most artiodactyl glands and their secretions is poorly understood.

Distribution

Artiodactyls are the most widespread of the ungulates. They are native to all continents, except for Antarctica and Australia, and are absent from the oceanic islands. However, introductions, primarily of domestic species, have been made around the world to areas outside their normal range, including to many small remote islands, where they have usually thrived.

Habitat

As Artiodactyls are widely distributed across much of the world, it is not surprising that they exhibit great variation in the habitats that they occupy. One factor that seems to define artiodactyl habitat is the presence of sufficient plant bio-mass to sustain their numbers. Depending on species, they inhabit most ecosystems and habitats from arctic tundra to tropical forest, including both hot and cold deserts, and they can be found at elevations ranging from valley floors to mountaintops. Four major patterns of habitat use occur. Some species (e.g., American pronghorn) specialize in exploiting open grasslands where they feed and at the same time use the excellent visibility to detect approaching predators. Rather than hiding, they simply move away relying on early detection and speed to avoid their predators. Other species (e.g., bighorn sheep, Ovis canadensis) specialize in exploiting open grasslands and meadows near the steep cliffs. This combination of habitats offers good foraging in the meadows with excellent security on narrow ledges and steep

terrain. Other species (e.g., okapi, Okapia johnstoni) dwell in forest or shrubland. In this habitat, they feed on the great variety of available plants, but also obtaining concealment from predators among the dense vegetation. The fourth pattern is shown by species (e.g., roe deer, Capreolus capreolus, from Europe or axis deer, Axis axis, from India) that inhabit the ecozone between forest and open areas. In the complex landscapes comprised of patches of forest or thickets juxtaposed with open areas, these species move between forest and open habitats, using each for different resources. They might use forest for shelter from the sun and for security cover from predators during the day, often resting along the forest edge where the have a clear view of predators and ready access to the concealment offered in dense forest. During the night, or in the early morning and late evening, they move into open areas and along the forest edge where they feed on lush forbs and other vegetation.

The habitats used by artiodactyls are linked to features of their biology and there are clear trends with body size and taxonomy. Small-to medium-sized artiodactyls often use relatively tall, dense vegetation that provides both food and cover (e.g., dik-dik, Madoqua spp.). Most members of the Caprinae (wild sheep and goats) inhabit mountain regions where they find security in steep cliffs and feed in adjacent grasslands. The hippopotamus (Hippopotamus amphibius) provides another contrast because members of this African species feed primarily on land at night, and grazing on vegetation growing away from the rivers and pools that they return to during the day.

Behavior

Few artiodactyls are truly solitary, and even though they may consist of only two or three members, most species live in groups. Typically, however, the sexes remain separate for most of the year (sexual segregation), with adult males living apart from adult females and young. The sexes often use different habitat types, different parts of the range, or both.

Group living seems driven primarily by predation pressure against which it confers several advantages, but probably the most important are dilution and vigilance. Sexual segregation is most likely driven by a trade-off between food requirements and predator avoidance. Males generally require more energy in order to grow large bodies and weapons for intraspecifc competition, and because of their larger body size and the fact that they have no vulnerable young to care for, they can use areas with higher predation risk than can females. Females are responsible for rearing the young, which are highly vulnerable to predators especially in the first few month of life. Females also need sufficient high-quality food for lactation, so they must balance predation risk for their offspring against their own food requirements. When the young are small, females tend to use areas with lower predation risk than do males, even if that means using areas with poorer quality or less abundant food.

Artiodactyls have a diverse array of weapons that they employ primarily in intraspecific interactions. The weapons often function not only for offence, but also have defensive functions. Antlers of deer are an excellent example of this dual function. Most cervids have antlers with several sharply pointed branches. Although such antlers are capable of inflicting serious injury, the forked branches also allow the animal to catch an opponent's antlers and so avoid injury. As a result of this dual offensive-defensive function, male deer fight head-to-head with antlers together as they try to twist each other off balance so they can stab the opponent with the antler points. Similar fighting strategies are seen in horned ruminants as well. Horns that grow in spirals, often with ridges, act in a similar way to branched antlers. The twists and ridges help to catch an opponent's horns, and the two often wrestle head-to-head, again trying to gain the upper hand and deliver an injurious blow.

Physical combat almost always carries a high risk for artiodactyls because, even though an individual might not be injured or killed, fights cost a lot of energy that could be used for mating or for feeding. Many artiodactyls use displays instead of actual fighting in an attempt to manipulate an opponent to withdraw. Displays are behavior patterns that are characteristically conspicuous and are usually directed at a conspecific. They include, for example, postures, vocalizations, and in some species, specialized morphological features have evolved as part of the display. Displays are used as threats, and as signals of dominance or submissiveness. Threat displays are typically aggressive intention movements, indicating cating a readiness to fight and almost always involve the weapons and stance of fighting style. For example, weapons such as antlers or horns may be pointed towards an opponent or be used to "attack" a nearby object such as a bush. Suids, which use their sharp canine teeth for fighting, threaten by grinding their teeth. Many artiodactyls also vocalize in aggressive situations (e.g., roaring by male bison, bellowing of domestic cattle, "bugling" of wapiti). When performing a dominance display, the animal tries to appear as large as possible and often they achieve this by standing sideways to an opponent (lateral or broadside display). Species such as chamois and kudu can raise the long hairs (piloerection) that run along the upper side of the neck and along the back, which in effect increases the apparent size of the displaying animal. Others such as some of the wild cattle (e.g., gaur, bison) have evolved elongated thoracic spines, which also increase the lateral profile. Submissive displays, on the other hand, appear to function by reducing aggression in an opponent, and it is common to see a submissive animal trying to make itself as small and non-threatening as possible. Frequently, subordinate males may even mimic the behavior of females.

Coloration patterns are also typically involved in displays and other social signals, but their connection to their "message" is not always obvious. For example, aggressive individuals will drop their ears as an indication of their behavioral state. In Nile lechwe (Kobus megaceros), the ears stand out noticeably against the black head and neck, further adding to the conspicuousness of this display. Other features of the pelage may have communication functions, and are mainly directed towards conspecifics. These characteristics are the result not only of different coat coloration, but also of different hair length. White-tailed deer (Odocoileus virginianus), for instance, raise their tails, exposing the long white hairs on the underside and over the rump, then bound off waving their tail from side to side as a warning signal to other deer that a predator is present. Other species such as pronghorn and Grant's gazelle (Gazella granti) have uncovered, prominent white rump patches that are permanent displays. They continuously signal among the group and are thought to help maintain group cohesiveness and alert members to disturbances. Also, coat characteristics may develop only in mature age and sex classes—in some Asiatic wild sheep and goats, only mature males develop large neck ruffs or beards, while in the Indian blackbuck antelope, males change from a reddish-to a black-colored coat on reaching maturity.

Feeding ecology and diet

Except for the Suidae and Tayassuidae, artiodactyls are obligate herbivores relying primarily on plants as their source of energy. The herbivorous diet of artiodactyls and the major adaptation to their anterior digestive system probably explains some of their success, because plants offer a diverse and abundant food source in most ecosystems. No mammal possesses enzymes capable of digesting cellulose or lignin, and so most obligate herbivores rely on microorganisms to breakdown these plant compounds. Within the artiodactyls, the most successful groups not only use microorganisms to help them breakdown plant tissues as do perissodactyls, but they also ruminate.

All artiodactyls have one or more chambers, or false stomachs, located just ahead of the true stomach, or abomasum. The pigs and peccaries have only one small chamber before the true stomach, hippos, camels, and tragulids have two, and Cervidae and Bovidae have three false stomachs (rumen, reticulum, and omasum) before the true stomach. Bacterial fermentation takes place in the first and largest chamber, the rumen, hence the alternative name for ruminants, the foregut fermentors. The large surface area of the cheek teeth with their selenodont enamel pattern, facilitate grinding of forage. The efficiency with which ruminant artiodactyls are able to digest plants is aided by their ability to ruminate, or chew their cud. In this process, the largest food particles move from the rumen to the reticulum where they are formed into a ball, or bolus, by the action of the honeycombed (reticulated) inner surface of this second chamber. The bolus is then regurgitated up the esophagus into the mouth, where it is once more chewed and mixed with saliva, before being swallowed once more. Together, these adaptations allow efficient digestion of vegetation and contribute to the success of artiodactyls as key components of ecosystems across much of the world.

Assisted by regrinding during rumination, the microorganisms are able to digest the smaller food particles, breaking them down into even smaller pieces. When reduced to a certain size, the particles move from the reticulum to the omasum through a small orifice that acts like a sieve and restricts the flow of food. In the omasum, most of the water is squeezed out of the food and reabsorbed through the folded and highly muscular walls. The now-drier food mass moves next into the abomasum, the true stomach where protein digestion begins. Most protein digestion, however, takes place in the intestines and the resulting amino acids are absorbed. The final step of digestion in ruminants occurs in the cecum, located towards the end of the gut where additional microbial fermentation takes place.

Ruminants are almost entirely dependant on the microorganisms for extracting nutrients from plants. Not only do the microorganisms allow the artiodactyls to extract energy from cellulose, but they are also the main protein source. The microorganisms use the plant protein to reproduce and, when they are transferred with undigested plant material from the rumen into the omasum and eventually the intestines, the ruminant digests the microbes, thereby recovering the protein that they contain. As a result, ruminants gain more valuable amino acids than if they relied on digesting plant proteins.

In addition to the benefits from the symbiotic relationship with the microorganisms for digesting their food, artiodactyls gain other advantages from rumination. They efficiently recycle nitrogen in the form of urea. During the fermentation process in the rumen, dietary protein is converted mainly to ammonia, which is either used by the bacteria or absorbed through the rumen wall and sent to the liver. Here, it is converted to urea, which is then returned to the rumen, either directly through the rumen wall or via saliva from the parotid glands. Another major advantage is that, after ruminants have filled their rumens, they can move to safer locations and habitats to digest their food. By selecting secure habitats to rest and digest, not only do they reduce predation risk, but also energy expenditures for locomotion are lowered.

While the majority of artiodactyls rely almost entirely on plants as a food source, there are well-documented records of this order, besides the Suidae, occasionally eating the eggs and young of ground-nesting birds as well as other sources of animal protein. These seem to be taken on a purely opportunistic basis and are a minor part of the normal diet, although it may be more frequent in the smaller-bodied artiodactyls.

There is a great range in body sizes among ruminants, and thus there are differences in both metabolic needs and the abilities to meet these needs. Small ruminants have relatively greater energy requirements than large species, and this influences the ways that they exploit plants. Although there can be exceptions, large species tend to be bulk feeders and thus less selective by gathering large quantities of low-quality vegetation. On the other hand, small species tend to be concentrate feeders and thus more selective by consuming plant species and parts that are high in nutrients and digestibility. Such feeding strategies facilitate division of resources and allow a diversity of artiodactyl species to coexist within the same ecosystem. This is especially evident in East Africa where dikdiks to African buffalo all form a species-rich community of herbivores.

Reproductive biology

All but the Suidae give birth to one, sometimes two young each year. Triplets are rare, but the pigs give birth typically to between four and eight young, with domestic pigs regularly giving birth to more than a dozen piglets per litter. Most species breed once each year, although in some tropical species there are two birth periods per year. The birth season is usually timed to coincide with onset of seasonal plant growth. As a result, most species give birth either in early spring in temperate and arctic regions or at the beginning of rainy season in tropics. The new flush of green nutritious vegetation at these times benefits milk production, which is the greatest physiological cost experienced by a healthy female. In addition, being born at the beginning of the plant-growing season allows the young a long period over which to grow while food is relatively abundant and of high quality. The faster the young grow, the lower their risk of predation.

The young of all artiodactyls are precocial, capable of walking and even running in some species within a few hours after birth. They can be classed into one of two broad types, depending on whether their mothers leave them during the day to feed elsewhere (hiders), or whether the young stay close to her (followers) during their first few weeks of life. Hider young have coat colors or patterns that help keep them concealed. Hider mothers lead their young to where they will leave them, and the young select the actual hiding site. The mother returns briefly once or twice during the day to nurse and clean her offspring. Later, when a hider young is older and more mobile, it accompanies its mother. Both are probably anti-predator tactics related to the visual density of the habitat and the size of the young. Species with the hider strategy tend to belong to smaller groups that inhabit habitats with suitable hiding places. Followers are typically larger species living in large groups and open habitats with few places to hide. Pigs show a variation of the hider strategy. The female just prior to birth builds a nest in which she has her litter of young. The piglets stay in the nest with the mother for a few days after parturition, then they are able to follow her.

The most common mating system is polygyny in which one male copulates with several females each mating season. In a few species such as the blue duiker (Cephalophus monticola), mated pairs may stay together most of the year, but such a mating system is the exception in artiodactyls. In many others, temporary mating pairs form and the male defends and courts a single female for as long as she is in estrous (e.g., Bison), or the male defends several females (harem) against other males (e.g., courting and mating with each female when she comes into heat). Both of these are forms of female defense polygyny. Another mating system, resource defense polygyny, is seen in many species such as the pronghorn (Antilocapra americana) or various African antelopes. In this system, a male defends a territory that attracts females because it contains valuable resources such as food or because it provides safety from predators. Females are also sometimes drawn to the male himself. Whether males hold territories during the rut depends on the economics of defense—whether the distribution and quality of resources that might attract females outweigh the costs of defending it. The most extreme form of mating territoriality is lekking, a behavior seen in fallow deer (Dama dama), topi (Damaliscus lunatus), and in several species of kob. In these species, large numbers of males congregate on a relatively small patch of ground where they defend territories that are no more than a few feet (meters) in diameter. When a female wanders onto one of these defended spaces, the males attempt to keep them there long enough to mate with them. Lekking does not occur in all populations of a species, but appears to depend, among other factors, on population density.

Conservation

A total of 168 artiodactyl species are listed in the IUCN Red List of threatened mammals. The listings statistics for this order are: Extinct: 7; Extinct in Wild: 2; Critically Endangered: 11; Endangered: 26; Vulnerable: 35; Near Threatened: 1; Lower Risk: 73; and Data Deficient: 13. Details of which species are threatened can be found at the IUCN Red List Web site, which is regularly updated.

Of the 155 species for which status has been determined, 53% (82 species) are in categories of conservation concern. Threats to artiodactyls range from over-harvesting (including poaching) to habitat loss and degradation (including deforestation, conversion to agricultural purposes), and competition with domestic livestock. Increased access such as roads and railways into to wildlife habitat exacerbates and precedes most of these threats. All, however, revolve around the central issue of increasing human demands for diminishing natural resources.

Significance to humans

Wild artiodactyls were the major large mammal prey for early hunter-gathers, and are still important today as sources of animal protein for many people who otherwise exist on subsistence agricultural production. Certain wild species (e.g., red deer, wild sheep and goats, kudu, antelopes, and African buffalo) are still much sought after by sport and trophy hunters. Rock and cave paintings and carvings attest to their long history of importance to humans; artiodactyls were the most common mammalian species depicted by the artists of the Paleolithic and later periods.

The most important domestic livestock species are cattle, sheep, goats, camels, pigs, all of which are artiodactyls. Sheep and goat were probably the first species to be domesticated after the dog, about 8,000–9,000 years ago. Domestic artiodactyls are key species in agriculture and food production, and as such are vitally important to all human societies throughout the world. Whether wild or domesticated, artiodactyls provide meat, fur, fiber, bones, medicinal products, antlers, and horns, while domestic species, in addition, are sources of milk, draught power, fertilizer, and wealth. Despite their usefulness, introductions of livestock, especially of domestic goats and pigs, to non-agricultural areas and islands (e.g., Isabela Island in the Galápagos) where they roamed freely, created feral populations, which, in turn, invariably lead to habitat degradation and conservation disasters.

Resources

Books

Byers, J. A. American Pronghorn: Social Adaptations and the Ghosts of Predators Past. Chicago and London: The University of Chicago Press, 1997.

Sowls, L. K. Javelinas and Other Peccaries: Their Biology, Management, and Use. 2nd ed. College Station: Texas A&M University Press, 1997.

Walther, F. R. Communication and Expression in Hoofed Mammals. Bloomington: Indiana University Press, 1984.

Periodicals

Gingerich, P. D., M. ul Haq, I. S. Zalmout, I. H. Khan, and M. S. Malkani. "Origin of Whales from Early Artiodactyls: Hands and Feet of Eocene Protocetidae from Pakistan." Science 293 (2001): 2239–2242.

Janis, C. M. "Evolution of Horns in Ungulates: Ecology and Paleoecology." Biological Reviews 57 (1982): 261–318.

Janis, C. M. "New Ideas in Ungulate Phylogeny and Evolution." Trends in Ecology and Evolution 3 (1988): 291–297.

Matthee, C. A., J. D. Burzlaff, J. F. Taylor, and S. K. Davis. "Mining the Mammalian Genome for Artiodactyl Systematics." Systematic Biology 50 (2001): 367–390.

Montgelard, C., F. M. Catzeflis, and E. Douzery. "Phylogenetic Relationships of Artiodactyls and Cetaceans as Deduced from the Comparison of Cytochrome b and 12S rRNA Mitochondrial Sequences." Molecular Biology and Evolution 14 (1997): 550–559.

Nikaido, M., A. P. Rooney, and N. Okada. "Phylogenetic Relationships among Cetartiodactyls Based on Insertions of Short and Long Interspersed Elements: Hippopotamuses Are the Closest Extant Relatives of Whales." Evolution 96(1999): 10261–10266.

Other

IUCN Red List Web site. <http://www.redlist.org>.

David M. Shackleton, PhD

Alton A. Harestad, PhD