Lagomorpha

(Pikas, rabbits, and hares)

Class Mammalia

Order Lagomorpha

Number of families 2

Number of genera, species 12 genera; 91 species

Evolution and systematics

The evolution and systematics of the Lagomorpha (pikas, rabbits, and hares) has a rich tradition of controversy, prompting one paleontologist to author a paper several decades ago entitled, "What, if anything, is a rabbit?" The problem, however, is not defining the limits of what constitutes a lagomorph (expanding "rabbit" to include pikas and hares), but rather determining the position of lagomorphs within the mammals. Lagomorphs represent a well-defined grouping, and although they were originally classified within the Order Rodentia, even in this alignment lagomorphs were separated into the Duplicendentata whereas the "true" rodents were classified as Simplicendentata. This distinction was based on the second small peg-like upper incisors that sit behind the primary incisors in all lagomorphs, while rodents possess only a single upper incisor.

In 1912, Gidley proposed that the duplicendentates be raised to a separate order, the Lagomorpha. The existence of the Lagomorpha and Rodentia orders has been adopted as standard terminology, but unfortunately this separation did little to solve the problem of relationship of lagomorphs with other mammals. For example, Gidley proposed the independence of the lagomorphs because he thought they showed significant differences from the rodents (above and beyond dentition) and believed they showed more affinities with ungulates, perhaps the Artiodactyla. Simpson, however, maintained that the lagomorphs and rodents should be recognized together and coined the term Glires to represent a clade made up of the two orders. According to this view, lagomorphs and rodents share a common ancestor, although Simpson was the first to admit that the relationship implied by Glires was "permitted by our ignorance, rather than sustained by our knowledge." Through the years the issue of whether or not lagomorphs belong in the Glires with the rodents was hotly debated, and lagomorphs were variously linked with a variety of other mammalian taxa.

We are now fortunate to have molecular techniques to complement an increased knowledge of fossil lagomorphs, and there has been a flurry of investigations in the past 10 years (many since 2000) that specifically address the evolutionary placement of the lagomorphs. Unfortunately, the results of these studies are as contradictory as in earlier times when we had fewer data. A majority of studies using molecular sequence data significantly support the Glires clade, incorporating the Lagomorpha and Rodentia. In these cases, Glires is apparently a sister taxon to Primates, Dermoptera (flying lemurs), and Scandentia (tree shrews). In addition, morphological data analyzed in a similar manner define Glires with 100% support. However, other molecular studies specifically reject the grouping of Lagomorpha and Rodentia, while others are ambiguous on the issue. One investigator put it this way: "The rabbit wanders about in the mitochondrial protein tree, undecided whether to join the carnivore-perrisodactylecet-artiodactyle clade, the primate branch, or neither." Other studies link lagomorphs with the tree shrews or the Xenarthra (armadillos). It is likely that the lack of support for the Glires clade in some molecular studies reflects poor taxon sampling within the lagomorphs and rodents. While the jury is out until there can be resolution among these various molecular approaches, a parsimonious conclusion is that the lagomorphs are indeed linked with rodents—as Glires—in their evolutionary history.

A complementary question is how long ago did the lagomorphs become an independent lineage? Again, here we are assisted by both molecular and paleontological data, and the

results are surprising. Until recently it was assumed that the major lineages of mammals diversified in the early Tertiary. Now, there is strong evidence from molecular data that lagomorphs were independent as long ago as the Cretaceous. Some reports using molecular sequence data indicate that the lagomorphs split from the rodents 64.5 million years ago (mya), others push the date back to over 100 mya. The variability in these molecular approaches, however, stems from their use of different genes, sampling, and methods, such that an unambiguous time of divergence between lagomorphs and rodents is not presently possible. In addition, a form with lagomorph characteristics, Alymlestes kielanae, has been uncovered in central Asia and dated to nearly 85 mya, thus pushing back the paleontological clock for lagomorphs. Thus, lagomorphs apparently became independent far earlier than had previously been assumed, and this independence likely occurred during the Cretaceous.

A significant fossil record of two rodentiform taxa (called eurymylids and mimotonids) is found in the Paleocene. The mimotonids appear to be primitive lagomorphs, whereas the eurymylids are linked with ancestral rodents (although in earlier treatments they were often classified as lagomorphs). These forms appear to be too advanced along their respective specialized lines to be ancestors, thus confirming that the Glires separated sometime during the Cretaceous. The most primitive representative of the mimotonids was Mimotoma, a rabbit-like animal similar to Alymlestes, but with a rabbit dental formula. Like rabbits it had two upper incisors, although the second incisor was still large and functional, while in modern-day rabbits it is small. Mimotoma was the likely ancestor to Mimolagus, an Eocene form that possessed many more lagomorph-like characteristics. Alymlestes, Mimotoma, and Mimolagus are all Asian forms, thus confirming an Asian center of origin for lagomorphs.

The first true rabbits (Leporidae) appear in the lower Eocene in Asia (Lushilagus, Shamolagus) and slightly later in North America (Mytonolagus). Lushilagus possesses teeth very similar to Mimotoma, and modern lagomorph dentition could easily have been derived from these teeth. These early forms lacked the limb proportions that characterize modern rabbits; they more closely resembled modern pikas. From this point it is possible to derive the lineages leading to both of the modern-day families of lagomorph, the Leporidae (rabbits and hares) and the Ochotonidae (pikas). The split into these two families occurred about 37 mya, or near the Eocene-Oligocene transition. By the middle Oligocene the first pika, represented by Desmatolagus gobiensis, was found in Asia, and other pikas soon appeared in Europe. Pikas would eventually flourish and reach their zenith in the Miocene. Geographically most pika evolution was restricted to Asia, Europe, and North America, but some forms reached Africa in the Miocene. Today, pikas are represented by a single genus, Ochotona, distributed in Asia and North America. Twentyfive extinct genera of ochotonids have been described, one of which, Prolagus, occupied Europe until historical times before becoming extinct.

By the early Oligocene a variety of true rabbits were found in Asia and North America, and the family would eventually spread throughout most of the world. Thirty-one extinct genera of leporids have been described, and today the family is represented by 11 extant genera.

The chapters on the Leporidae and Ochotonidae detail the evolution of these families, respectively. However, one important observation highlights the evolution of the lagomorphs. There are relatively few lagomorph species compared with the closely related rodents (over 2,000 rodents versus only 91 lagomorphs), and this discrepancy has never been adequately explained. Furthermore, morphologically there has been significantly less innovation (fewer specialized adaptations) in lagomorphs than in rodents. The term lagomorph means "hare shaped" and this description adequately serves to portray all species in the order.

Physical characteristics

The key characteristic of the lagomorphs, the one that led them to be classified originally in the duplicidentata, is the presence of a second peg-like upper incisor that nestles in behind the first large continually growing incisor. A third incisor forms, but is lost before birth or shortly thereafter. There is a single layer of enamel in the front incisors of rabbits in contrast to the double layer in rodents. This enamel layer surrounds the incisor on all sides (unlike in rodents) and is not colored by stored pigments, as are rodent incisors. The lower incisors in lagomorphs can occlude directly with the main upper incisors (as in rodents), but they can also "slide" behind the upper ones to press against their flat surface, thus allowing an efficient cropping mechanism. Canines are absent, and there is a gap (the diastema) between the incisors and the molars. The occlusal plane of the cheek teeth is not parallel with the zygomatic arch in lagomorphs, whereas this surface and the arch are parallel in rodents. The cheek teeth are rootless and hypsodont with two transverse ridges (unlike the several transverse ridges on rodent cheek teeth). Pikas have 26 teeth; leporids, 28. Lagomorphs have a fenestrated skull one with areas of thin lattice-like bones, a feature particularly well developed in some leporids.

Lagomorphs, especially the leporids, are quick on their feet and/or fast runners. Leporids have long legs and large hind feet, and the tibia and fibula are fused distally to add strength and reduce weight to the leg. The soles of lagomorph feet are covered with hair (except the distal-most toe pads in pikas). The hairs on the soles of the feet are rectangular when viewed in cross-section. The foot posture is digitigrade while running, but plantigrade during slow movements. No lagomorphs are able to grasp food with their paws. Ears are huge to relatively large (even pika ears are large for their body mass compared with most rodents), and tails are short and, in pikas, not visible. Lagomorphs have soft rather long fur, and the color is normally reddish to gray-brown. The gut is large, in particular the caecum, and all lagomorphs practice coprophagy (reingestion of feces). A pseudo-cloaca is present such that there is one opening for reproduction, urine and feces.

General body shape differs between representatives from the two families. Pikas are egg-shaped, roughly 5–8 in (13–20 cm) long, and weigh 3–10 oz (80–300 g). Leporids are more angular and larger, ranging in length from 10–30 in (25–75 cm) and in weight from 14 oz to 13.2 lb (0.4–6.0 kg).

Distribution

Lagomorphs are distributed around the world, as native or introduced species. The pikas once had a broad distribution across most of Eurasia, North America, and into Africa. Currently, however, they are found only in the mountains of the inter-montane west in North America and in Alaska, and across much of Asia primarily in the high mountains of Central Asia, but also south into the northern Middle East and across Russia from the Urals to the East Coast. An isolated population also occurs on Hokkaido in northern Japan.

The leporids currently have a far greater geographic distribution, being found naturally throughout the world with the exception of Australia, New Zealand, and other islands of Oceania, Madagascar, southern South America, and most of Amazonia. The European rabbit (Oryctolagus cuniculus) and the European hare (Lepus europaeus) have been introduced widely in particular to areas not naturally occupied by rabbits. Thus, Australia, New Zealand, southern South America, and over 500 oceanic islands now are home to these invaders.

Habitat

Pikas occupy two distinctly different habitats. The two North American pikas and roughly half of the species in Asia live in rocks or boulder fields and do not dig burrows. These pikas utilize vegetation found in meadows at the talus edge or growing in small patches within the rocks. In special circumstances rock-dwelling pikas are "fooled" into occupying areas with the general physiognomy of rock piles, but which are not, such as heaps of fallen logs.

The remainder of the pikas, all Asian species, live in meadow, steppe, shrub, or open desert environments where they dig burrows. Rarely are two burrowing species found in the same locality, but a burrowing pika can occur in meadow habitat that abuts the habitat of a talus-dwelling pika.

The true hares (genus Lepus) in general prefer open country high arctic tundra, steppe, agricultural pasture, tropical savanna, and desert. Within these habitats some form of cover (shrubs or rocks) is needed for protection from predators (in particular, birds of prey). Hares also use cover for protection from the elements, and generally run into the open to avoid predators. A few Lepus spp. live in forests, such as the snowshoe hare (L. americanus), Manchurian hare (L. mandshuricus), and some populations of mountain hare (L. timidus).

No single vegetative community typifies the habitat of cottontail rabbits (genus Sylvilagus). Some are found in marshy areas (S. aquaticus, S. palustris), many occupy forested regions (e.g., S. brasiliensis, S. cunicularius, S. graysoni, S. insonus), and other brushy situations (e.g., S. bachmani, S. floridanus, S. mansuetus, S. nuttallii, S. transitionalis). The closely related pygmy rabbit (Brachylagus idahoensis) requires big sagebrush (Artemisia tridentata) habitat for its existence.

Several rabbits are endemic to Africa. The riverine rabbit (Bunolagus monticularis) specializes on dense riparian growth along seasonal rivers in the central Karoo region of South Africa. All three species of rockhare (genus Pronolagus) are true to their common name, being restricted to

rocky situations in association with grass or scrub vegetation. The bunyoro rabbit (Poelagus marjorita) also is associated with rocky outcrops occurring in moist savanna or open shrub woodlands.

The hispid hare (Caprolagus hispidus) of India and Nepal is dependent on early successional riverine communities, typically comprised of tall dense grasslands. Both Nesolagus spp. from Sumatra and southeast Asia occupy dense tropical forest. The Zacatuche or volcano rabbit (Romerolagus diazi) of the highlands of central Mexico lives in open pine forests with an understory of thick bunch grass called zacaton. The zacaton is required for food, cover, and protection for this species. The Amami rabbit (Pentalagus furnessi) of Japan lives in primary forest, but also has been found to occupy forest edges and secondary forests. Finally, the common European rabbit (Oryctolagus cuniculus) is a denizen of open grasslands with well-drained, loosely compacted soils for constructing their warrens, although it is eminently adaptable and found in nontypical situations.

Behavior

Social organization, territoriality, and behavior

The pikas have two sharply contrasting forms of social organization. Those species that inhabit rocky or talus habitats are extremely unsocial. In the American pika (Ochotona princeps), males and females hold separate territories of comparable size and rarely interact. Rock-dwelling pikas in Asia tend to live in pairs on a communal territory, but they still avoid one another and engage in few social encounters. Territory size for rock-dwelling pikas is variable, and largely dependent on the quality of vegetation adjoining the talus; the lower the quality of surrounding vegetation the larger the territory. For most species territory size is large, compared to the size of its occupant(s), and average sizes range from approximately 600–2400 yd² (500–2,000 m²). Most rock-dwelling pikas are rather pugnacious and chase conspecifics whenever they are encountered. Neighboring adult males and females suppress this aggressive urge some of the time, and adults do not always chase their own young.

In contrast, burrowing pikas are among the most social of mammals. These animals live in family burrow systems functioning as a family territory. As the summer breeding season progresses and young from sequential litters are weaned, the density on these family territories becomes high. In the plateau pika (Ochotona curzoniae) approximately 10 families occupy each hectare, and each family may be comprised of up to 30 pikas, yielding regional densities of 120 per acre (300/ha). Affiliative social interactions are frequently expressed among family members, including such behaviors as nose-rubbing, sitting-in-contact, boxing, wrestling, and grooming. Aggression, generally in the form of a long chase or fur-flying fight, is reserved for pikas that wander off of their family territory and into the domain of their neighbors.

Variability in social organization is also seen in the leporids. Most hares and rabbits live solitary lives and are non-territorial. Some form temporary feeding aggregations, and the Arctic hare (Lepus arcticus) can be seen in huge herds. Territories are defended by the largely solitary European hare (L. europaeus). Most representatives of the Sylvilagus spp. occupy relatively stable overlapping home ranges of only a few acres, and several species have a male dominance hierarchy which controls the social structure of their population.

Unlike any other leporid, the European rabbit (Oryctolagus cuniculus) is extremely social. Defended territories are usually small (approximately 2.5 acres [1 ha]) and made up of a "warren"—an interconnected maze of burrows. A warren usually consists of six to 12 adults controlled by a dominant male who sits at the top of a strict linear hierarchy of dominance. Most rabbits remain in the area of their warren for life.

Communication and senses

The dominant form of communication in lagomorphs is olfactory—all species have a keen ability to detect odors. In turn, all lagomorphs have glands on their cheeks, chin, and/or groin areas that are used to rub pheromones on their coat during grooming, or to deposit scent marks on rocks or shrubs. Urine and feces are also used to transmit olfactory messages. Individual animals broadcast these pheromones to advertise their reproductive status or to demarcate their territorial boundary.

Very few lagomorphs are vocal. Some hares and rabbits communicate by thumping their big hind feet, and hares can expel a deep grumbling sound. The piercing shriek given by leporids when in distress is legendary. But, only the Zacatuche (Romerolagus diazi) and pikas (genus Ochotona) are truly vocal. Rock-dwelling pikas utter a restricted repertoire of calls, just a short call used to advertise their territory and alert neighbors of the presence of predators and a long-call (or song) given by males during the breeding season. Burrowing pikas express a rich variety of calls, including whines, trills, and muffle-like sounds, that complement their social milieu, and males also give a breeding season long-call.

While vocal communication is restricted in most lagomorphs, they still possess an acute sense of hearing. Hares in particular, but all lagomorphs, have large ears that assist in detecting predators.

Pikas have small eyes and do not seem to rely significantly on their sense of vision. On the other hand, leporids are known for their large laterally set eyes that provide a nearly circular field of vision. This arrangement provides for restricted visual acuity (which the animals do not need, as their food is sedentary), but enhances their ability to detect motion from all angles in order to avoid the approach of predators. Many leporids, in particular those living in open habitats, flash the white underside of their fluffy tails during flight to alert conspecifics of the presence of predators. Interestingly, species living in forested habitats have dark tails and do not use this form of communication.

Activity patterns

With the exception of the nocturnal steppe pika (Ochotona pusilla), all pikas are diurnally active. When temperatures are warm, pikas tend to restrict their activity to early morning and late afternoon hours.

Most leporid activity occurs at night, although many species can also be seen active during the day particularly at dawn and dusk. For example, one might classify the European rabbit (Oryctolagus cuniculus) as noctural, but its preferred feeding time is dawn.

Migratory movements

No lagomorphs migrate. The term is sometimes associated with rare mass movements of some hare species (for example the European hare) following highly unusual climatic events but these cases do not represent true migration.

Feeding ecology and diet

Lagomorphs are, with rare exception, strict herbivores. Unlike many rodents, they are unable to hold or process food

with their paws, instead relying on the clipping of vegetation and side-to-side mastication of vegetation using only their mouths. Lagomorphs are rather generalized herbivores, with a diet consisting primarily of grasses and herbs, but also fruits, seeds, roots, leaves, buds, and bark of trees. As no lagomorphs hibernate, their feeding ecology must accommodate the need to harvest vegetation year round, or in the case of pikas to store food when access to vegetation is restricted.

Most pikas live in northern or high altitude environments blanketed by snow during winter. They adapt to these conditions by harvesting vegetation during summer, a time of abundance, and storing it into a cache or hay pile to serve as a source of nutrition during winter. The folk story that pikas lay out their hay on rocks to cure before carrying it to their hay pile is untrue; pikas harvest their hay with great economy, sometimes making hundreds of trips per day to deposit their loads directly on their hay pile.

Although generalized herbivores, pikas can be highly selective of the foods they eat. During summer most rockdwelling pikas maintain a heavily grazed zone in the meadow adjoining the talus (on which they hold their territories). This zone allows pikas to graze continually on growing grasses, and also to better see approaching predators. At the same time pikas forage for their hay piles at greater distances from the meadow-talus edge, and they primarily select forbs to carry back to their cache. Forbs are larger and more economical to carry than grasses, although grasses can also be gathered up and deposited on haypiles. Plants selected for haying are generally higher in nutrition than non-selected plants, and in most cases they are less likely to be poisonous. The exception is that some rock-dwelling pikas harvest plants that, while poisonous, also inhibit bacterial growth in the hay piles, thus preventing them from rotting. This is an apparent win-win situation for the pikas, as these plants help to preserve the hay piles and later can be eaten after the toxic chemicals degrade.

Pika hay piles can be huge or sometimes inconspicuous when tucked under large boulders. There can be variability in how hay piles are constructed even within a single population. Burrowing pikas that do not have rocks under which to tuck their hay sometimes make giant stacks over a yard high. These are exposed when the snow otherwise covers the landscape, and Mongolian herdsman in the range of the Daurian pika (Ochotona dauurica) take advantage of these efforts and graze their livestock preferentially in areas occupied by pikas. Some pikas apparently do not make hay piles, and normally these species live in areas without snow where they can forage year-round. Even pikas that make hay piles often construct snow tunnels to allow foraging on nearby vegetation blanketed by snow.

One of the only known instances in which a lagomorph survives by eating meat is found in an isolated population of the collared pika (O. collaris). These pikas live on nunataks, or small islands of rock in the middle of a sea of ice, protruding from the Seward Glacier in the Yukon, the world's largest non-polar ice field. It is remarkable to find pikas in this environment, and even more so that they can survive on the few plants that also hang on in this bleak place. These pikas eat the brains from birds that die while flying overhead and fortuitously fall on the nunataks giving them their slim margin for survival.

Leporids are generally feeding opportunists, eating a smorgasbord of plants from those that are available in the habitats in which they live. Plant resins have been identified as a deterrent in lagomorph herbivory and may play a role in the 10-year population cycle of snowshoe hares (Lepus americanus). Close inspection of the area surrounding creosote bushes (Larrea tridentata) in the deserts of the southwestern United States yields many clipped but uneaten branches. Apparently each branch contains different levels of alkaloids, and black-tailed jackrabbits (L. californicus) prune the shrub, taste to assess the alkaloid level, eat the palatable branches, and discard the remainder.

Given a selection of plants, most leporids choose those which are the most succulent, particularly during times of water stress. They also prefer plants in the pre-reproductive or early reproductive stages of development that have the greatest nutritive value. Like pikas, leporids select plants that are comparatively higher in moisture and crude protein. Given that plant quality and availability changes dramatically with the seasons, so does the diet of rabbits and hares. Most jackrabbits, for example, show preferences for shrubs in winter and for grasses and forbs in spring and summer. The tendency of rabbits and hares to gravitate toward the most nutritious plants also is responsible for their love of cultivated areas. Here agricultural crops, bolstered with nutrients from fertilizers, represent a cornucopia to lagomorphs, and often result in dramatic increases in their population density. On the other hand, in natural conditions hares often are close to starvation when available food may be covered by snow and they are unable to harvest twigs sufficiently to meet their needs. In some areas it has been determined that hares will starve in winter when the diameter of twigs used for browse is greater than 1 in (3 mm).

Special dietary adaptations

Because generalized herbivores, such as lagomorphs, have such difficulty in acquiring food of a sufficient quality in terms of necessary vitamins and micro-nutrients they have been forced to develop specialized dietary adaptations. Lagomorphs possess a huge digestive system that appears specially constructed to deal with the large quantities of plant material they eat, much of which is difficult to digest. In particular, they feature a giant caecum up to 10 times larger than the stomach that branches off from the gut between the small and large intestines. This organ, its surface area enlarged by numerous divisions separated by a spiral fold of skin that runs through it, hosts a rich culture of bacteria and other microorganisms. Here, partially digested food (that not absorbed by the animal during passage through the small intestine), is broken down by these microorganisms, and in the process various vitamins (in particular vitamin B complex) and microbial proteins are manufactured. To be able to utilize these products, lagomorphs practice what is called coprophagy which literally means feces-eating. A soft feces is excreted from the caecum (called a caecotroph) and reingested. The reingested soft feces can then be digested in the stomach and small intestine yielding up to five times as many vitamins as in the original food. This process is such an integral part of lagomorph biology that if prevented from reingesting soft feces, a rabbit may develop malnutrition or die.

The caecotrophs, or soft feces, contrast with the normal hard round dry pellets characteristic of lagomorphs. These soft and hard feces are produced by a mechanical separation process, dependent on the size of food particles, in the small intestine. Fine food particles are shunted into the caecum, and large particles, basically those of poor quality, form the hard pellets and are passed quickly. When the separation mechanism ceases to act, fermented caecotrophs are excreted. The difference between the two feces types is not due to whether or not the food has passed once or twice through the gut, as is commonly assumed; some foods may be recycled numerous times. Within the leporids, there are two types of caecotroph: capsules (a spherical shape coated with a tough mucous membrane) found generally in rabbits and amorphous (without a surface membrane) most commonly found in hares.

Most of the literature on lagomorphs states that soft feces are excreted at night (sometimes even termed "night feces"), and that hard pellets are never eaten. Recent studies, however, show that lagomorphs regularly eat hard feces and that the timing of coprophagy, with respect to hard and soft feces, can be complex. Most feeding takes place at night in leporids, and during that time the separation mechanism is activated so that hard feces are formed and fine food particles are shunted to the caecum. In the morning, when animals cease feeding, hard pellets remain in the large intestine. These are excreted and reingested, after which soft feces are formed and reingested until early afternoon. Then the separation

mechanism kicks in again to form hard feces that reach the anus in a few hours and are reingested in the afternoon. Thus, leporids feed on fresh food and ignore feces during the night, and excrete both hard and soft feces during the day and reingest these. This process is not as well known in pikas. Some caecotrophs are not eaten directly (perhaps when pikas have an abundance of fresh nutritious food and they are not necessary to achieve sufficient nutrition), and are deposited near the hay pile. These may be eaten later, or some grow a fungus after which the entire mass is reingested.

Reproductive biology

Most of our general knowledge of reproduction in lagomorphs comes from investigations on the European rabbit (Oryctolagus cuniculus). Rabbits are known to be reflex, or induced, ovulators. Females may come into heat and be attractive to males, but the act of copulation is needed to stimulate ovulation, which occurs about 12 hours after mating. It is assumed that this pattern is followed in other lagomorphs. Another interesting twist in lagomorph reproductive biology is the phenomena of "superfetation." In European hares (Lepus europaeus), a female in late pregnancy can go into heat, mate, ovulate, and be impregnated and thus carry two litters of different age in her uterus at one time. This process naturally can lead to a rapid increase in the local population in a short time. Most pikas exhibit a post-partum estrus, thus initiating sequential litters back-to-back, with the same effect of truncating reproduction into as short an interval as possible—a particularly effective strategy given the short alpine summers experienced by most pika species.

Another interesting aspect of reproduction in lagomorphs is their apparent lack of parental care—in particular, the infrequency of nursing bouts initiated by mothers. Termed "absentee parental care" by Eisenberg, most mothers visit their young to nurse only about once every 24 hours. Fortunately lagomorph milk is extremely rich and the young are able to survive these long intervals between meals. This strategy may have arisen for mothers to avoid bringing their young, exposed in a shallow form, to the attention of predators.

Pikas do not express elaborate courtship or mating behavior. For both talus-dwelling (Ochotona princeps) and burrowing (O. curzoniae) pikas, males generally approach females, sniff the genital area briefly, and mount. Copulation lasts only a few seconds after which the pair separate. Rock-dwelling pikas tend to be monogamous; Asian forms live in pairs, and males and females in the American species generally occupy neighboring territories and show some familiarity with each other. Burrowing pikas live in family groups that also define their mating system. However, over-winter mortality is high and capricious, thus the availability of males and females within family territories can vary across the landscape. Most families begin the breeding season with one male and one female, thus demonstrating true monogamy. Some families have more adult females than males and are polygynous, whereas the reverse, a family with more adult males than females, yields a polyandrous mating system. All three types of mating systems can be found in adjoining family territories. Young pikas are born beneath tons of rock or deep in burrow systems, making observations of parental care difficult. Some captive studies and anecdotal field observations indicate that while pika mothers visit their young infrequently, they nurse more often than in the "absentee" system of most leporids. When young rock-dwelling pikas are weaned and appear on the talus, they are treated aggressively by their parents. Normally young avoid confrontations by choosing to be active at times when their parents are inactive and confining their movements to areas near the borders of adult territories. The opposite is true of newly weaned burrowing pikas. Fathers, and to a lesser degree mothers, are highly attentive toward their offspring and engage in numerous affiliative behaviors with them.

Reproduction is highly seasonal in all pikas beginning at the end of winter and extending through early summer. Timing and length of breeding season depends on altitude, latitude, that year's climate, and whether the species is a rock or burrowing form. Rock-dwelling pikas initiate two litters each year, although normally only one is successful. Litter size is small, generally three young (range of one to five), and not all of these are successfully weaned. Animals first breed as yearlings; gestation is 30 days. In contrast, burrowing pikas initiate many (up to five) sequential large litters (range of one to 12), and weaning success appears to be high. In some burrowing forms young mature quickly and breed initially in their season of birth. Gestation is approximately 20–21days. Thus, reproductive performance is greater in all dimensions in burrowing versus rock-dwelling pikas.

The most elaborate courtship pattern in lagomorphs has been described in the European hare. First, large mating groups aggregate from which animals seemingly pair off. Apparently these partners are faithful and live together for about one month. The extended courtship involves repeated chases and approaches, tail flagging, and contact. Copulation finally ensues, although lasting for less than 10 seconds. The pair separate with a giant leap by the female used to throw off the male. Vigorous pursuit and repeated copulations may follow. Most other hares and rabbits express a muted version of this behavior, and in some instances, copulation occurs without any preliminary courtship. In European rabbits mating is based on the dominance hierarchy within a warren; the mating system in most other species is either unknown or assumed to be based on either a dominance hierarchy or random encounters.

Hares are precocial (being born fully furred and with their eyes open) at birth. This condition follows a relatively long gestation period of about 40 days. Coupled with the lack of attention given young during the lactation period, there appears to be little in the way of parental care expressed toward young hares. Rabbits have a shorter gestation period of about 30 days, and their young are altricial (born without any fur and with their eyes closed) at birth. Mothers construct a nest, sometimes in a protected burrow dug for this purpose, lined with hair from their own belly and plant material to secure their young. The European rabbit enters a social world in the tightly knit warren, thus benefits from behaviors of parents and others. Most other rabbits, however, do not receive substantial parental care and independently enter the world following weaning.

Leporids are legendary for their reproductive potential. Indeed, many species have many large litters each year, and young may reach sexual maturity at a relatively early age. However, lagomorphs live in a wide variety of ecosystems, and many of these are stressful and energy limited. In these conditions some species may not be as fecund. In the far north, where the summer breeding season is short, native hares (Lepus othus, L. arcticus) normally conceive only one large litter per year. In desert situations where some hares (L. californicus, L. alleni) may face a shortage of resources over an extended breeding season, litter sizes may consist of only one to three young, although they may produce four to seven litters each year. Latitude, and thus its effect on season length, may significantly influence litter size. For example, the Eastern cottontail (Sylvilagus floridanus) produces larger litters in the northern part of its range (average is 5.6), with a steady decline in litter size to the southern limit of the species (average is 3.1). Thus, seasonality and productivity of the habitat appear to be major influences on the fecundity of leporids.

Conservation

Currently the official IUCN Red List of Threatened Species lists 19 species of lagomorph as Threatened (IUCN categories of Critically Endangered, Endangered, or Vulnerable) out of 79 species for which complete assessments have been made (eliminating those species with Data Deficient or Not Evaluated; the IUCN/SSC Lagomorph Specialist Group has not had the opportunity to assess several new species recently described or assigned). The resulting 24% level of endangerment is equal to that for the class Mammalia as a whole. However, changes in assignment which are proposed, but not yet finalized, would change these numbers to 25 threatened species out of 86, or an endangerment level of 29%.

Most critical in this analysis is the level of endangerment found in those genera of lagomorphs with two or fewer species. The Lagomorpha contains seven monospecific genera and one genus with two species. Within this assemblage of the most phylogenetically unusual lagomorphs six of eight genera (75%), and seven of nine species (78%), are threatened with extinction.

Some of the most endangered mammals in the world are lagomorphs. The silver pika (Ochotona argentata) is known only from one 0.9 × 1.2 mi (1.5 × 2.0 km) patch of scrub located in the isolated Helan Shan mountains of central China. Similarly, the Ili pika (O. iliensis) lives in isolated cliffs in northwestern China, and several recent expeditions to assess its population have failed to relocate it at its type locality. Over 100 years past from the finding of Koslov's pika (O. koslowi) until it was recently rediscovered, and its habitat in central China is subject to widespread alteration. The pygmy rabbit (Brachylagus idahoensis) has declined severely throughout its range; in 2002, it disappeared from five of six known localities in the Columbia River population. The number of surviving riverine rabbits (Bunolagus monticularis) is estimated to be as low as 500 animals, its preferred habitat is disappearing, and none of its habitat is governmentally protected. Populations of the hispid hare (Caprolagus hispidus) are declining in the face of dramatic habitat loss throughout its range in Nepal and India. The Tehuantepec jackrabbit (Lepus flavigularis) is found in only three isolated populations in southern Mexico, each with only a handful of individuals. The only striped rabbits, two Nesolagus spp., are essentially unknown. The Sumatran rabbit (N. netscheri) has only been recorded a handful of times, and the only sightings in the past several decades were on film of two individuals captured by an automatic camera-trap in 1998. The newly found (first described in 2000) Annamite rabbit (N. timminsi) is best known for being found in a market in Laos as meat; its ecology is unknown. The Amami rabbit (Pentalagus furnessi) of Japan is the world's only black rabbit. Only 3,000 individuals remain on the two islands they inhabit and are threatened by an introduced mongoose and rampant deforestation. The volcanic highlands of central Mexico surrounding Mexico City host the 6,000 remaining zachatuche (or volcano rabbits [Romerolagus diazi]). Found on only 16 small patches of habitat, the zacatuche is being threatened by logging, burning of the zacaton grass on which it depends to enrich regrowth for cattle grazing, and thatch collection of zacaton for baskets. Only three specimens are known to science of the Omiltimi rabbit (Sylvilagus insonus) from the West Coast of Mexico, although in 1998 a barnyard dog retrieved another. Rigorous searches throughout its putative range already a protected area have failed to produce any additional sightings.

Significance to humans

Lagomorphs are economically and aesthetically important to humans in many ways. The pikas, normally living in remote pristine settings high in mountains or on the plateaus of Asia, represent wildness. The secretive yet engaging nature of these diurnally active creatures are enticing to ecotourists. Pikas have little history of direct economic importance to humans. They are too small to be utilized as food, although at times their soft fur has been used to make felt in central Asia. Also in central Asia, the soft feces of pikas is put through a distilling process and dried into a product called "mumio" that can be dissolved in water as a folk remedy to assist with the healing of broken bones or rheumatism. Some of the burrowing pikas are thought to compete with human economic interests and are poisoned. The Afghan pika (Ochotona rufescens) sometimes occupies agricultural areas, eating wheat or other crops and damaging apple, walnut, and other economically important trees. Other species (Pallas's pika [O. pallasi], Daurian pika [O. dauurica], plateau pika [O. curzoniae]) are believed to compete with livestock or to damage range lands. As an example of these control efforts, during the past four decades the plateau pika has been poisoned cumulatively over 80,000 sq mi (200,000 sq km) in Qinghai Province, China. Another perspective, however, on the role of the plateau pika is that it serves as a major keystone species for biodiversity on the Tibetan Plateau. When these pikas are poisoned other native species of endemic birds and predators that depend on the pikas for food disappear. The pikas also function to recycle soil and reduce erosion on degraded lands. While some control efforts continue, the tide is turning and this beneficial role of the plateau pika is being more widely acknowledged in China.

Leporids provide sport hunting, food, and fur worldwide. The cottontail rabbit (genus Sylvilagus) is the principal game animal in the United States; millions are hunted for sport each year. The pelt is sometimes used for clothing, and the meat is considered a delicacy. Snowshoe hares (Lepus americanus) have been a major component of the fur trade, particularly in Canada. Records of their pelts from the logs of the Hudson Bay Company extend back to early 1800s. Other hare species, both in North America and throughout the world, are also hunted for food and sport. In North America hares are not considered as desirable as cottontails. The European hare (L. europaeus) has declined in numbers and importance as a game species in recent years, and similar declines have been noted across Asia for other hare species. In Argentina, where it has been introduced, over six million European hares are hunted annually, and others are exported to Italy for sport hunting there.

Rabbits and hares also form an important link in ecological food chains; many predators rely on the abundance of the non-hibernating leporids in their diet, particularly during winter. One key example of this phenomenon is the linkage of numbers of the lynx with those of the snowshoe hare, which range from high to low population levels in a 10-year cycle. Leporids can also cause damage to ecosystems when their numbers are high, either girdling trees or consuming forage that could otherwise be available to livestock. Rabbits and hares are attracted to crop lands, reach high densities in these areas, and concomitantly are also considered an agricultural pest in certain areas.

The greatest damage done by a lagomorph has resulted from the human folly of introducing the European rabbit (Oryctolagus cuniculus) to areas throughout the world where there were no lagomorphs. The most dramatic example of such an alien introduction occurred in Australia. Here, 24 rabbits were introduced in 1859, and they rapidly increased and spread throughout most of the continent. In 1950 there were an estimated 750 million rabbits in Australia, and the damage that the rabbits have caused is legendary. Not only has the livestock industry been impacted, but the degradation to the habitat has led to the loss of many of Australia's unique native flora and fauna. The enterprising Australians have tried nearly everything to rid their land of this pest. The biological control agent, myxomytosis, initially proved to be highly effective, killing nearly all animals in most populations. However, rabbits have developed immunities and rebounded from this treatment. Additional innovative control techniques are in development.

The domestication of the European rabbit in southern Europe or Northern Africa in Roman times has led to a close connection between people and rabbits. The domestic rabbit now has over 100 varieties and serves as a lovable pet, and breeding stock for meat and fur.

Resources

Books

Averianov, A. O. "Mammals from the Mesozoic of Kirgizstan, Uzbekistan, Kazakhstan and Tadzhikistan." In The Age of Dinosaurs in Russia and Mongolia, edited by M. J. Benton, M.A. Shishkin, D. M. Unwin, and E. N. Kurochkin. Cambridge: Cambridge University Press, 2000.

Chapman, J. A., and G. A. Feldhamer, eds. Wild Mammals ofNorth America. Baltimore: Johns Hopkins University Press, 1982.

Chapman, J. A., and J. E. C. Flux, eds. Rabbits, Hares and Pikas:Status Survey and Conservation Action Plan. Gland, Switzerland: IUCN, 1990.

Cheeke, P. R. Rabbit Feeding and Nutrition. Orlando, FL: Academic Press, Inc., 1987.

Hoffmann, R. S., and A. T. Smith. "Lagomorphs." In Mammal Species of the World: A Taxonomic and Geograhic Reference, Vol. 3, edited by D. E. Wilson and D. M. Reeder. Washington DC: Smithsonian Institution Press, In Press.

Li, C-K, R. W. Wilson, M. R. Dawson, and L. Krishtalka. "The Origin of Rodents and Lagomorphs." In Current Mammalogy, Vol. 1, edited by H. H. Genoways. New York: Plenum Press, 1987.

Myers, K., and C. D. MacInnes, eds. Proceedings of the WorldLagomorph Conference. Guelph, Canada: University of Guelph, 1981.

Smith, A. T. "Population Structure in Pikas: Dispersal versus Philopatry." In Mammalian Dispersal Patterns: The Effects of Social Structure on Population Genetics, edited by B. D.

Chepko-Sade and Z. T. Halpin. Chicago: University of Chicago Press, 1987.

Thompson, H. V., and C. M. King, eds. The European Rabbit: The History and Biology of a Successful Colonizer. Oxford: Oxford University Press, 1994.

Periodicals

Averianov, A. O. "Phylogeny and Classification of Leporidae (Mammalia, Lagomorpha)." Vestnik Zoologii 33 (1999): 41–48.

Cao, Y., M. Fujiwara, M. Nikaido, N. Okada, and M. Hasegawa. "Interordinal Relationships and Timescale of Eutherian Evolution as Inferred from Mitochondrial Genome Data." Gene 259 (2000): 149–158.

Dobson, F. S., A. T. Smith, and X G. Wang. "Social and Ecological Influences on Dispersal and Philopatry in the Plateau Pika." Behavioral Ecology 9 (1998): 622–635.

Dobson, F. S., A. T. Smith, and X. G. Wang. "The Mating System and Gene Dynamics of Plateau Pikas." Behavioural Processes 51 (2000): 101–110.

Hedges, S. B., and S. Kumar. "Divergence Times of Eutherian Mammals." Science 285 (1999): 2031a.

Hirakawa, H. "Coprophagy in Leporids and Other Mammalian Herbivores." Mammal Review (2001): 61–80.

Huchon, D., O. Madsen, M. J. J. B. Sibbald, K. Ament, M. J. Stanhope, F. Catzeflis, W. E. deJong, and E. J. P. Douzery. "Rodent Phylogeny and a Timescale for the Evolution of Glires: Evidence from an Extensive Taxon Sampling Using Three Nuclear Genes." Molecular Biology and Evolution 19(2002): 1053–1065.

Killian, J. K., R. R. Buckley, N. Stewart, B. L. Munday, and R. L. Jirtle. "Marsupials and Eutherians Reunited: Genetic Evidence for the Theria Hypothesis of Mammalian Evolution." Mammalian Genome 12 (2001): 513–517.

Landry, S. O. Jr. "A Proposal for a New Classification and Nomenclature for the Glires (Lagomorpha and Rodentia)." Mitteilungen aus dem Zoologischen Museum in Berlin 75(1999): 283–316.

Liu, F-g. R., and M. M. Miyamoto. "Phylogenetic Assessment of Molecular and Morphological Data for Eutherian Mammals." Systematic Biology 48 (1999): 54–64.

Kumar, S., and S. B. Hedges. "A Molecular Timescale for Vertebrate Evolution." Nature 392 (1998): 917–920.

Murphy, W. J., E. Elzirik, W. E. Johnson, Y. P. Zhang, O. A. Ryder., and S. J. O'Brien. "Molecular Phylogenetics and the Origins of Placental Mammals." Nature 409 (2001): 614–618.

Smith, A. T., and J. M. Foggin. "The Plateau Pika (Ochotona curzoniae) is a Keystone Species for Biodiversity on the Tibetan Plateau." Animal Conservation 2 (1999): 235–240.

Smith, A. T., and M. L. Weston. "Ochotona princeps."Mammalian Species 352 (1990): 1–8.

Smith, A. T., and X. G. Wang. "Social Relationships of Adult Black-lipped Pikas (Ochotona curzoniae)." Journal of Mammalogy 72 (1991): 231–247.

Stoner, C. J., O. R. P. Bininda-Emonds, and T. M. Caro. "The Adaptive Significance of Coloration in Lagomorphs." Biological Journal of the Linnean Society (In Press).

Swihart, R. K. "Body Size, Breeding Season Length, and Life History Tactics of Lagomorphs." Oikos 43 (1984): 282–290.

Organizations

IUCN Species Survival Commission, Lagomorph Specialist Group. Department of Biology, Box 871501, Arizona State University, Tempe, AZ 85287-1501 USA. E-mail: a.smith@ asu.edu Web site: <http://www.ualberta.ca/dhik/lsg>

IUCN Species Survival Commission, Red List Programme Office. Web site: <http://www.redlist.org>

Andrew T. Smith, PhD