Chiroptera

(Bats)

Class Mammalia

Order Chiroptera

Number of families 19 living families (18 recognized by some researchers)

Number of genera, species 192 genera; 1,057 species

Introduction

Bats are nocturnal, coming out at night. They are the only mammals capable of true (meaning, flapping) flight, because the other so-called flying mammals (for example, squirrels, lemurs, and sugar gliders) glide, they do not fly. Today, the diversity of bats is astonishing, with more than 1,000 species making them second only to rodents as the most diverse group of mammals. Although some bats have remarkable faces and behavior, wings are the most conspicuous features of the flying bats. Upon landing, bats immediately fold their wings so they appear to shrink in size. Small size is another distinctive feature of bats. While a few species weigh more than 3.5 oz (100 g) as adults, most weigh less than 1.7 oz (less than 50 g), and the majority less than 0.9 oz (less than 25 g). The smallest bats in the world (hog-nosed bats, Craseonycteris thong-longyai, family Craseonycteridae from Thailand and Myanmar) weigh 0.07 oz (2 g) as adults. The largest, the Indian flying foxes (Pteropus giganteus) from India, Pakistan, and Southeast Asia, weigh 52.9 oz (1,500 g).

Chiroptera means hand (cheiro) and wing (ptera). Bat wings are folds of skin supported by elongated arm, hand, and finger bones, and attached to the sides of the body. In most cases, bats' thumbs are relatively free of the wing membranes and bear claws, which are absent from the fingers. Flying foxes and their allies (family Pteropodidae) usually have claws on their second fingers, but some species (dawn bats, genus Eonycteris, and naked-backed fruit bats, genus Dobsonia) lack these claws. Second fingers with claws occur in some fossil bats.

Measurements made with Doppler radar indicate that bats fly about 6.5–49.2 ft (2–15 m) per second. Bats use nine pairs of muscles to power flight. Muscles that power the down-stroke are located in the chest, and those responsible for the upstroke are located in the back. Although some bats have quite muscular forearms, their wing bones tend to be lightly muscled. In most bats, the folds of skin (wings) enclose some connective tissue, nerves, and blood vessels. Some free-tailed bats (Molossidae) also have sheets of muscle in the wing membranes. In mechanics and aerodynamics, the flight of bats is very similar to that of birds. The passage of air over the airfoil section of the wings generates lift. Movements of the wing tips generate propulsive thrust.

Bats show considerable variation in wing shape and flying abilities. In many species, the wings are relatively broad, providing good lift. Shorter-winged species tend to be more maneuverable than longer-winged ones. Many species of flower-visiting bats and some species that take animal prey from the ground can hover. While some species of bats can take off from the ground, those with longer, narrower wings cannot.

Although both can fly, bats differ from birds. While living birds such as ostriches, emus, and penguins, and fossils like elephant birds have lost the ability to fly, there are no living or fossil flightless bats. Bats have teeth, while living birds do not. Bats give birth to live young, while birds lay eggs. Since teeth are heavy, having them at the front end of a flying animal could create aerodynamic problems. Additionally, laying eggs could be more efficient and less costly for a flying animal than bearing live young. The diversity of birds (more than 8,000 species) suggests that their approach is more successful than that of bats (1,000 species).

In birds, the wings do not involve the hind limbs as they do in bats. The hind limbs of bats tend to be spindly and poorly muscled, and many bats are not mobile on the ground. Most birds are much more mobile on the ground, and their robust hind legs reflect this reality. Mobility in the air, on the

ground, and beyond (as for penguins) may partly account for differences in diversity between bats and birds.

In addition to the obvious (i.e., bird wings are made of feathers, while bat wings are folds of skin), there are other differences between these animals. In bats, the division of power generation across nine pairs of muscles means that they are thin in profile through the chest. In birds, two pairs of muscles power flight: one the down-stroke, the other the up-stroke. Both sets of muscles are located on birds' chests and the upstroke muscles operate by a pulley system. A thin profile through the chest allows bats to squeeze into narrow cracks and crevices that serve as places to spend the day (day roosts). While a bird typically has a prominent keel on its breastbone (sternum), this feature is absent in most bats and never as well developed as it is in birds. Birds have wishbones (furcula), bats do not.

In most bats, the thumbs are free of the wings, appearing there as claws. In some bats, notably thumbless ones (family Furipteridae) and some ghost bats (genus Diclidurus, family Emballonuridae), the thumbs are greatly reduced in size and may lack claws. At the other extreme are the very long thumbs of vampire bats (Desmodus rotundus). Vampire bats' thumbs act like "throwing sticks," giving the bats extra leverage for taking off from the ground.

Bats' wing membranes usually join along the side of the body, but in two groups they meet in mid-back. The naked-backed bats belong to species in two families, Old World fruit bats (genus Dobsonia, family Pteropodidae) and naked-backed moustached bats (two species in the genus Pteronotus, family Mormoopidae). The function of the naked back remains unknown.

Wing membranes may attach to the bats' hind legs, extending as far down as the fifth toe of the hind feet. In other species, they attach higher up, at the ankle or knee. Carnivorous bats typically have an interfemoral membrane (between the hind legs) that encloses all or part of the tail. On the tail side, the calcar, a cartilaginous structure protruding from the ankle, supports the back edge of the interfemoral membrane. In flight, the interfemoral membrane acts as a rudder and also reduces oscillations of the body through each wing-beat cycle. But interfemoral membranes are not essential to bats: some plant-visiting and blood-feeding species have very narrow interfemoral membranes or lack them completely.

Most bats have tails. But while tails of some (e.g., mouse-tailed bats, Rhinopomatidae, and some Pteropodidae) are long and slender, others (e.g., free-tailed bats, Molossidae) are short and thick. Tails may or may not extend to the end of the interfemoral membrane. Some bats lack obvious tails.

The diversity of bats is reflected by the variety of trophic (ecological) roles they fill in ecosystems. While most species are mainly insectivorous, others eat plant products (fruit, leaves, seeds, nectar, or pollen). Other bats eat animals such as fish, frogs, birds, and even other bats. The most infamous of bats are the blood-feeding vampires, arguably the most remarkable of mammals. The ecological diversity of bats is reflected in their anatomy and behavior. The cheek teeth (molars and premolars) of carnivorous bats are quite different to those of frugivorous (fruit-eating) bats. Nectar-and pollen-feeding bats have teeth more specialized for crushing food, while the vampires have scalpel-sharp razors.

The facial features of bats reflect their remarkable diversity. Bats also are diverse in their selection of roosts, places they spend the day, and by the social systems that develop in these places.

Evolution and systematics

In spite of their small and delicate skeletons, bats have a long fossil record, something that was not obvious to biologists even 50 years ago. By the Eocene, there were species in

at least 10 families of bats, four now extinct. Eocene bats are known from the United States, Germany, and Australia, as well as Pakistan.

It is assumed that bats evolved from nocturnal, arboreal, insectivorous animals that lived in forests. The combination of their small size, delicate skeletons, and the forest conditions make the ancestors of bats unlikely candidates for fossilization. There are no fossils of animals that are part bat, part something else, but it is speculated that a shrew-like animal would be a good candidate as a remote ancestor of bats.

The fact that bats appear fully formed and diverse in the Eocene means that it is not known when they first appeared. The very first bats could have shared the skies with the last of the pterosaurs, overlapping in time with the last dinosaurs. Furthermore, although the fossil record suggests a high level of variety, there are relatively few fossil bats and, for most living families, there is no fossil record.

Living species of bats are classified in two suborders: the Megachiroptera (flying foxes and their relatives, family Pteropodidae), which are the fruit-and flower-visiting bats of the Old World tropics, and the Microchiroptera, which include all of the other bats. The two groups are easy to distinguish. The Pteropodidae have dog-like faces, simple ears, and most have claws on their second fingers. Microchiroptera (18 families) lack claws on their second fingers, do not look like dogs, and their ears (and related structures) are more complex. The teeth of megachiropterans tend to be more specialized than those of microchiropterans (excepting vampire bats). Microchiropteran specializations for flight, particularly in the shoulder girdles, are more complex than those of megachiropterans. While the flying foxes and their relatives use flight to get from one place to another, many microchiropteran species feed on the wing and require higher levels of agility and maneuverability.

From the late nineteenth century, some biologists have questioned the closeness of the relationship between Megachiroptera and Microchiroptera. Two theories appeared. The monophyletic theory holds that the two suborders of Chiroptera are more closely related to one another than either is to any other group of mammals. The diphyletic theory proposes that the Megachiroptera are more closely related to some other group of mammals than they are to Microchiroptera. The neural details of how their eyes connect to their brains indicated that while megachiropterans were like primates, the microchiropterans were like all other mammals. Additional evidence about morphology and genetics has been presented. By the year 2000, the monophyletic theory was more accepted than the diphyletic one. New information could reopen and extend the debate.

Physical characteristics

In general anatomy and physiology, bats are like other mammals. Wings make bats distinct and flight imposes some physiological constraints that make them different in degree from other mammals. For example, the hearts of bats are larger than those of other mammals of comparable size. This difference reflects the higher capacity of the circulatory system associated with flight.

Bats are warm-blooded and, like other animals in this category (birds and mammals), expend energy to maintain body temperatures higher than ambient (surroundings). Bats face a challenge with respect to heat and energy, reflecting the realities of flight and small size. Flying bats shed excess heat generated by contractions of flight muscles, while roosting bats often conserve heat. In flying bats, wings act like radiators because direct connections between small arteries and small veins facilitate shedding heat. To conserve heat, bats roost in places that are at least warm if not hot, saving them the costs of thermoregulation, for example, shivering to keep warm. In temperate areas in summer, bats often use the warmest available roost sites, for example, in attics or tree hollows exposed to direct sunlight for much of the day, or heated rock crevices around hot springs.

Heterothermy, the ability of a warm-blooded animal to let its body temperature follow the ambient across some range, is another way that some bats conserve energy. Many species of plain-nosed (Vespertilionidae), horseshoe (Rhinolophidae), and free-tailed (Molossidae) bats are heterothermic, while other bats are not (e.g., slit-faced bats, Nycteridae; Old World leaf-nosed bats, Hipposideridae; and false vampire bats, Megadermatidae). The ability to hibernate (body temperatures measuring below 50°F [10°C] to freezing for a prolonged period) is extreme heterothermy. Heterothermy excuses bats from paying the costs of maintaining their body temperatures above ambient. Heterothermy allows bats (and other animals) to wait out periods of inclement weather (short-term torpor) or to hibernate (long-term torpor).

Distribution

Absent only from very remote oceanic islands, the high Arctic, and the Antarctic, bats are extremely widespread. For the most part, heterothermic species are the bats of temperate regions.

Some species of bats migrate hundreds of miles (kilometers) to avoid inclement seasons, but there is detailed knowledge in only a few cases. Schreiber's long-fingered bats (Miniopterus schreibersi) in Australia, noctules (Nyctalus noctula) in Europe, or Brazilian free-tailed bats (Tadarida brasiliensis) in parts of the New World are species whose seasonal movements have been documented by band recoveries. Seasonal appearances and disappearances of straw-colored fruit bats (Eidolon helvum) at different locations in Africa suggest migrations, and the same patterns have been used to support the proposal that red bats (Lasiurus borealis), hoary bats (Lasiurus cinereus), and silver-haired bats (Lasionycteris noctivagans) migrate in North America. In many other species, the seasonality of captures suggest migrations, but there are not documented movements of individuals (e.g., wrinkle-faced bats, Centurio senex).

The migrations of Brazilian free-tailed bats, like those of many insectivorous birds, allow individuals to remain active year-round because they follow their food supply (insects). Migrations of other bats (e.g., little brown bats [Myotis lucifugus],

Indiana bat [Myotis sodalis], gray myotis [Myotis grisescens], and Daubenton's bats [Myotis daubentonii]) are from summer habitats to hibernation sites. Underground sites (caves or abandoned mines) often are used for hibernation because they provide consistent above-freezing temperatures, often combined with high relative humidity. There are differences in hibernation site requirements (temperature, relative humidity) between species. In temperate areas, other species of bats (e.g., big brown bats, Eptesicus fuscus) use hibernation sites that are close to their summer roosts. Species like noctules hibernate in hollow trees.

Habitat

Bats can be found in virtually every habitat available from rainforests to deserts, montane forests to seasides. Bats have two basic habitat requirements: roosts, or places to spend the day or hibernate, and places to feed. The actual selection of roosting or foraging habitat depends on the species and the time of year.

Roosts of bats can be divided into four broad categories: hollows, crevices, foliage, and "other." Hollows, situations where the roosting bat hangs free by its hind feet, may be inside trees, rocks (caves, mines), buildings, or even birds' nests. An unexpected discovery was of round-eared bats (genus Tonatia, family Phyllostomidae) roosting in hollows in the bases of arboreal termite nests. Crevices and cracks, situations where the bats' venter is against one surface (and its back may be close to the other), occur in rocks, trees (under bark or in wood), and buildings. Bats roosting in foliage may hang from branches of trees, or among or under leaves. The "other" category includes bats roosting in unfurled leaves or in tents.

In the New World, three species of disk-winged bats (genus Thyroptera) roost in unfurled leaves of plants like heliconia or bananas. These roosts are available for about a day, because as the leaves grow they unfurl, obliging the bats to move regularly to new leaves. Suction disks on the wrists and ankles allow the bats to move about on the smooth leaf surfaces. In Africa, rufous mouse-eared bats (Myotis bocagei) and African banana bats (Pipistrellus nanus) roost in unfurled banana leaves. These bats lack suction disks.

In the Neotropics, India, and Southeast Asia, a number of species of bats roost in tents. Tents, usually leaves modified by biting, shelter bats from direct sunlight and rain. One or two species of short-nosed fruit bats (genus Cynopterus, family Pteropodidae), one species of plain-nosed bat (a yellow bat, genus Scotophilus), and about 18 species of New World leaf-nosed bats (family Phyllostomidae) use tent roosts. In the New World tropics, individual tents can last for several months and be occupied by a succession of bats. There is relatively little information about how bats build tents. In India, male lesser short-nosed fruit bats (Cynopterus brachyotis) build tents that are occupied by the tent-builder and groups of females and their dependent young.

Flattened skulls are examples of morphological specializations associated with roosting in narrow spaces or in roosts with small entrances. Good examples occur among free-tailed bats (genera Platymops, Sauromys, and Neoplatymops) that roost

under rocks. Bamboo bats (plain-nosed bats, genus Tylonycteris) roost inside the hollows of bamboo stems. They enter these roosts through small holes made by bruchid beetles. These bats have very flattened skulls. Bats roosting on rough surfaces (e.g., under stones) may have wart-like projections on the forearms (e.g., Platymops, Neoplatymops). Species roosting on very smooth surfaces can have suction disks that are best developed in disk-winged bats, either from the New World (family Thyropteridae) or in Madagascar (family Myzopodidae).

Roosting bats readily exploit artificial structures as roosts. People may find bats roosting in their homes. Around buildings, bats can be found roosting in attics or eaves, behind shutters, even among the folds of rolled up patio umbrellas. Bats also roost in the expansion cracks of bridges, a famous example being the Congress Avenue Bridge in downtown Austin, Texas, United States. Bats frequently roost in abandoned mines and in active underground water conduit systems. Today, it is common for people to erect bat houses or bat boxes to provide additional roosting opportunities. Some bat houses have resident bats, while others do not. It remains to be determined if bat populations are limited in size by the availability of roosts.

Behavior

Among mammals, flight is a behavior unique to bats. Two other behaviors, echolocating and hanging upside down, are associated with bats, but not characteristic of them. Not all bats echolocate and not all bats use echolocation the same way. Furthermore, the echolocation calls of many species of bats are ultrasonic, which, by definition, is beyond the range of human hearing. But many species of bats echolocate with sounds readily audible to people.

Bats also use vocalizations in many social situations, and their social calls are often quite audible to people. Male fruit bats in Africa (African epauletted bats [genus Epomops]; epauletted fruit bats [genus Epomophorus]; hammer-headed fruit bats [Hypsignathus monstrosus]) call to attract females. Pipistrelles (Pipistrellus pipistrellus) use harsh-sounding calls to discourage others from feeding in small patches of insects. Greater spear-nosed bats (Phyllostomus hastatus) have group-specific screech calls that keep group members together. Researchers are only just beginning to explore the many ways in which bats use vocalizations.

When roosting, many bats hang upside down. This distinctive behavior makes take-off very easy: the bat just lets go, drops, and starts to fly. Hanging upside down may reflect specialization of the forelimbs as wings and attachments of wing membranes to the hind legs. Many other species of bats roost horizontally, their abdomens against the substrate. These bats, notably some species of free-tailed bats, are quite mobile on the ground, readily running or crawling. Compared to bats that probably never operate on the ground (e.g., some horseshoe bats), free-tailed bats have robust hind limbs, particularly thighbones (femora). Still other bats, for example, Spix's disk-winged bats (Thyroptera tricolor, family Thyropteridae), roost head-up.

Roosting upside down could present problems for hygiene. To relieve themselves (urinate or defecate), bats hanging upside down turn head up to minimize the chances of soiling themselves. Bats are very clean animals, spending time every day grooming. Grooming bats use their tongues, teeth, and toe claws. The claws are used to comb fur and teeth to remove groomed materials from the claws. Bats regularly lick their wings, reaching both sides by turning the wings inside out. Grooming bats also lick their fur. Bats roosting in groups may groom one another. Grooming also maintains coat condition in bats. Combing with the claws of the hind feet also may dislodge ectoparasites such as bat flies (families Streblidae, Nycteribiidae, order Diptera), fleas (order Siphonaptera), bedbugs (order Hemiptera), or lice (order Mallophaga). It is not clear if combing or licking affects mites, which can also be common ectoparasites of bats.

The level of behavioral interactions among roosting bats depends on the situation and the setting. Although a hibernaculum may harbor tens of thousands of individuals, the atmosphere is very quiet as the bats are asleep. This contrasts sharply with the levels of activity in other situations where many bats roost together. These roosts resound with vocalizations as neighbors jostle one another or vie for position. Some bats roost in large aggregations, for example, the several million Brazilian free-tailed bats roosting in Frio Cave in Texas. Many other bats roost alone or in small groups. Red and hoary bats roost alone or in small groups (a female and her dependent young), while Spix's disk-winged bats may roost alone or in groups of up to 10. It is not known where many of the 1,000 or so species of bats roost and there is no information about the social settings in which they operate.

Large aggregations of bats often attract predators because the small size of each bat is more than balanced by their large numbers. In many parts of the world, it is common to see birds of prey hunting among groups of bats emerging from (or returning to) roosts. The aerial chases are obvious, but on the ground other predators also exploit the rich patches of prey presented by large numbers of bats. The list includes mammals such as raccoons, skunks, foxes, civets, house cats, and even a variety of snakes. Although many predators take bats when the opportunity presents itself, few specialize on bats. Bat hawks (Macheirhamphus alcinus) are exceptions. These birds occur in Africa and Southeast Asia and feed heavily on bats. The same may be true of some bat-eating bats, but these are little-studied and details are lacking about the role bats play in their diets.

In many tropical species of bats, reproduction is an organizing influence in roosts. Typically, groups include a single adult male with a group of females and their young. In species forming larger colonies, for example, gray-headed flying foxes (Pteropus poliocephalus), males may be in contact with females only during the period of mating. In tropical species, groups of bachelor males, individuals not holding a territory suitable for breeding, are common (e.g., greater spear-nosed bats). In many temperate species, there is general isolation of males and females in summer, with the latter forming large nursery colonies, sites where they bear and raise young.

Feeding ecology and diet

The combination of small size and high metabolic rates means that bats consume enormous quantities of food. The heart of a flying little brown bat beats about 1,200 times a minute, reflecting the rate at which it burns energy. The same bat, having landed, has a heartbeat rate of less than 300 per minute. During seasons when they are active, little brown bats (like other bats) eat about half their weight in food every night. Nightly, fruit-eating bats may handle three times their weight in food. Lactating females have higher energy demands and nightly eat more than their weight in food.

Consumption of large amounts of food often means that bats eat a variety of prey species, whether insects or fruit. While some insectivorous bats may eat more soft (e.g., moths, flies) than hard (beetles, bugs) prey, there is little evidence of specialization by prey species. Insectivorous bats should not be thought of as consumers of mosquitoes. However, some smaller species, for example, Bodenheimer's pipistrelle (Pipistrellus bodenheimeri) from the Middle East, are known to regularly eat mosquitoes.

Bats normally do not eat food they find distasteful. The list of such prey includes at least arrowhead frogs and insects (like tiger moths) protected by unpleasant chemicals. While insectivorous and frugivorous bats learn to avoid food that has made them sick, this taste aversion does not occur in vampire bats. Whatever their food, bats have ways of avoiding ingesting indigestible materials. From insects, they typically bite off and drop wings and legs, from bats and birds, the wings, or cellulose fibers from leaves and fruit. Insects pass quickly through the digestive tracts of bats, 20–30 minutes for little brown bats. Weight reduction translates into lower costs of flight. There is no evidence that bat populations are limited in size by the availability of food.

Insect-eating is a recurring lifestyle in bats, from tropical South America to Alaska, northern Scandinavia to tropical Africa, Malaysia to Tasmania. While most species of insectivorous bats hunt flying insects and use echolocation to detect, track, and assess their targets, others (gleaners) take prey from surfaces such as foliage or the ground. Some bats such as New Zealand lesser short-tailed bats (Mystacina tuberculata) show great mobility on the ground where they search for food. Their menu includes animals as well as nectar and pollen.

Gleaning bats eat more than flying insects, consuming a wider range of prey, including walking insects and arthropods that do not fly. Larger gleaning bats take a wider range of prey by size than smaller ones. Gleaners such as pallid bats (Antrozous pallidus) from western North America eat large scorpions and centipedes, Jerusalem crickets, and even small pocket mice (genus Perognathus). Larger gleaning bats like the Australian false vampire bat (Macroderma gigas), spectral bat (Vampyrum spectrum), and large slit-faced bats (Nycteris grandis) also eat birds and even other bats.

Aerial-feeding bats tend to take smaller prey than gleaning bats. Among bats, it is rare to find aerial-feeding species

taking vertebrate prey. The only known exception is the greater noctule (Nyctalus lasiopterus) from southern Europe. For at least part of the year, this 1.7 oz (50 g) bat preys on migrating birds.

Many species of animal-eating bats hunt along the water's surface. Called "trawlers," these bats (often in the family Vespertilionidae, the plain-nosed bats) have enlarged hind feet with which they gaff small fish. Mexican fishing bats (Myotis vivesi) from Baja California, and Rickett's big-footed bat (My-otis rickettii) from southern China are two examples. The best-known fishing bat is the greater bulldog bat (Noctilio leporinus, family Noctilionidae) from Central America, South America, and the West Indies. Other trawling bats do not have such large hind feet, but still take the occasional fish and even mosquito larvae. This list includes Daubenton's bat, pond bats (Myotis dasycneme), long-fingered bats (Myotis capaccinii), and large-footed myotis (Myotis adversus). Fish eating has been documented in two other bats, large slit-faced bats from Africa

and greater false vampire bats (Megaderma lyra) from India and Southeast Asia. These bats do not have enlarged hind feet and are thought to catch their fish directly in their mouths—but to date, they have never been observed fishing.

Other bats eat frogs. Most is known about the fringe-lipped bat (Trachops cirrhosus, family Phyllostomidae) of the New World tropics. This bat listens for the songs male frogs use when courting females, and uses them to find prey. Fringe-lipped bats grab singing frogs directly in their mouths and eat all of them, starting from the head. In south-central Africa, large slit-faced bats prey heavily on frogs, but there is no indication of their using the frogs' songs to find their prey. The same is true of heart-nosed bats (Cardioderma cor) that occur further north in Africa, or of greater false vampire bats in India. Large slit-faced bats also eat frogs from the head down, invariably leaving one leg from the ankle, and the toes of the other foot.

Throughout the tropics, some species of bats get food from plants. Included on the menu are fruits, seeds, leaves, nectar, and pollen. In the Neotropics, the plant-visiting bats belong to the family Phyllostomidae. In the Old World tropics, the bats are in the family Pteropodidae. The two families show remarkable convergence in structure and behavior.

When eating fruit or leaves, bats typically chew their food thoroughly, all the while using their tongues to rub mashed food against prominent ridges on the roofs of their mouths (palates). During this process, the bats suck vigorously, removing the digestible parts of fruit and leaves before spitting out pellets of indigestible fibers.

Flower-visiting bats obtain sugars from nectar and proteins from pollen. Some Neotropical bat flowers have ultrasonic reflectors that guide nectar-feeding bats to nectar and pollen. By drinking their own urine, nectar-feeding bats create acidic conditions in their stomachs, ideal for digesting pollen. Some flower bats also obtain protein from insects.

The most infamous of bats are the blood-feeding vampires. There are three species: vampire bats, hairy-legged vampires (Diphylla ecaudata), and white-winged vampires (Diaemus youngii), all in the family Phyllostomidae. These bats only eat blood they obtain by making shallow bites on a prey's skin. The bites do not penetrate large blood vessels such as arteries or veins. Vampire bats use razor-sharp upper incisor teeth to remove a 0.2-in (5-mm) diameter divot of skin, creating a wound that bleeds readily. The bats enhance bleeding by the actions of their tongues and saliva. The saliva of vampire bats contains chemicals that inhibit the body's defenses against bleeding, including anticoagulants, anti-agglutinants, and chemicals that inhibit local vasoconstriction. Each vampire species appears to be a "one-stop shopper," getting each blood meal from one prey. The bats ingest about 2 tablespoonfuls (25 ml) of blood. Blood represents less than 10% of the mass of a bird or mammal, meaning that only victims larger than 4.4 lb (2 kg) are suitable hosts for vampire bats. Within two minutes of beginning to feed, vampire bats start to urinate. The urine consists mainly of the plasma from the current blood meal; therefore, it is very dilute. This is the bat's way of ridding itself of indigestible material.

Reproductive biology

In their life histories, bats are long-lived with low reproductive output. In the wild, individually marked bats (little brown bats and greater horseshoe bats [Rhinolophus ferrumequinum]) have survived more than 30 years, and females have the capacity to produce one young per year. In Britain, greater horseshoe females appear to have young only every second or third year. Furthermore, 70% of these bats born in any year do not survive their first winter. The litter size in bats is typically one, though a few species bear twins at least some of the time, and another few, notably red bats, may have litters of even three or four.

During birth, female bats turn heads-up to allow gravity to assist with the birth process. The ligaments holding the two halves of the pelvic girdle together are capable of great flexibility to allow birth. Young are born back-end first. Newborn bats are huge compared to their mothers: single young

are 25–30% of their mother's postpartum mass. Young consume their own weight in milk every day and grow quickly. In some bats, for example, little brown bats (0.3 oz [8 g]) from North America, young reach adult size (forearm length) by about age 18 days. By then, their milk teeth have been replaced by adult dentition, they have started to fly, and insects first appear in their diets. Big brown bats (0.5 oz [15 g]) take about 28 days to reach this stage, and young vampire bats continue to nurse until they are six months old.

Young bats have huge appetites for milk, which is expensive to produce. Female bats roosting in nurseries with hundreds or even thousands of others use a combination of spatial memory, voice, and odor to recognize their own young. This ensures that her young receives enough milk and maximizes its chances of survival. The challenge of recognizing her young depends upon the female's situation. A red bat roosting only with her own young, has a different task than the Daubenton's bat roosting with tens of other Daubenton's bats. Female Brazilian free-tailed bats with nurseries numbering in the millions have a huge challenge in this regard—one they regularly meet and overcome.

Gestation periods in bats range from 60–100 days, and in most bats, fertilization follows copulation. Most species of bats are monestrus, with females having one reproductive event per year. Some tropical species are diestrus, have two reproductive events per year, and females in a few species (e.g., lesser-crested mastiff bats, Chaerephon pumila) may bear up to five young per year (one per estrous cycle).

Some species of bats extend the time between mating (typically polygynous) and birth. Sometimes fertilization follows copulation, but development or implantation of the fertilized egg is delayed, extending the gestation period. This occurs in some New World leaf-nosed bats (e.g., California leaf-nosed bats, Macrotus californicus) and plain-nosed bats (some populations of Schreiber's long-fingered bats). The other approach, known from plain-nosed bats and horseshoe bats, is to delay fertilization. In this case, females store sperm in the uterus after copulation. Storage can last from less than 20 days in some tropical species, to almost 200 days for north temperate forms. Delayed fertilization does not extend the gestation period. Extension of the time between mating and birth ensures that young are born at the most productive (in terms of food) time of the year.

Conservation

There are three categories of threats to the survival of bats: the general threat of habitat destruction, specific threats to habitats or habitat features important to bats, and threats to bats themselves.

General loss of habitat is the most pressing threat to the survival of most species of bats. Habitat loss typically reflects human population density either directly (urban sprawl) or indirectly (harvesting of resources that generates habitat destruction or disruption). Most species of bats occur in tropical areas, often those with rapidly increasing human populations. Extensive harvesting of rainforests occurs in many parts of the world, no doubt affecting the survival of bats. Detailed information is lacking about the distribution of many species of bats, and there is no accurate information about the sizes of their populations. Nor is it known which habitats or habitat features are vital to bats. This level of ignorance means that specific data cannot be provided about the impact of habitat loss on most of the world's bat species.

Some habitat disruption, specifically forestry or other operations that remove roosts used by bats, can imperil their survival. In other cases, programs to close caves or old mines in the interest of human safety can deprive bats of vital roost sites. In still other cases, habitat connections such as hedgerows are vital for bats like lesser horseshoe bats (Rhinolophus hipposideros) so that agricultural and other land-use practices can threaten the survival of some bats. In the United States, species of bats listed as Endangered experienced population declines as the result of disturbance in their cave roosts. For gray myotis, disturbances were to both nursery and hibernating colonies. For Indiana bats, disturbances were to hibernating animals. Bats are known to survive hibernation by going long periods without arousing. In little brown bats, each arousal from hibernation costs the energy that would support 60 days of hibernation. Survival of bat species that regularly hibernate depends on protecting them in their hibernacula.

Public perception can jeopardize bats. The association of bats with blood-feeding and diseases like rabies can make them the objects of persecution. Continued access to roosts for bats using buildings depends on human attitudes. When bats are perceived as dangerous, human occupants of their building roosts are more likely to take steps to evict them. If bats have moved into buildings in the wake of loss of natural roosts, then eviction may be tantamount to a death sentence. The level of protection accorded bats varies considerably. In the United Kingdom and much of Europe, bats enjoy considerable protection. In the United States and Canada, protection is not nearly as effective. In these countries, bats have more often been associated with rabies, coloring their status with respect to protection, people, and public health. In too many countries, bats have little practical or effective protection.

Their small size means that bats are rarely hunted by people, although in some parts of the world, bats are regular components of people's diets. On some South Pacific islands, hunting pressure has driven some species of bats to extinction. The situation in Guam, for example, demonstrates how the use of bats as festive food affected neighboring populations. After bat populations in Guam had been hunted to very low levels or to extinction, bats were then imported from as far away as the Philippines and New Guinea.

Significance to humans

For the most part, bats interact little with people although many species exploit human structures as roosts or feed in rich patches of food people create. But bat-people interactions are not entirely benign. Bats are commonly associated with two diseases that can afflict humans, histoplasmosis and rabies.

Histoplasmosis, a fungus disease of the lungs, can be contracted when people inhale the spores of the fungus Histo-plasma capsulatum. In warmer parts of the world, these spores are often associated with bat droppings. Their occurrence in bird droppings, including those of pigeons and chickens, is much more widespread. Although histoplasmosis typically gives flu-like symptoms, it can cause severe illness and even death. By wearing a mask that filters out particles larger than 10 microns (0.0004 in), people working in areas where they could encounter the spores of H. capsulatum can avoid exposure.

Rabies, a disease of the nervous system, is caused by a lyssavirus. Normally associated with mammals, rabies is usually fatal. Rabies virus tends to accumulate in the saliva of infected animals. Transmission usually occurs by biting when saliva with virus enters a wound. Today, rabies is an uncommon disease in the developed world. Elsewhere, rabies is usually associated with dogs and some other Carnivora and annually accounts for 30,000–70,000 human deaths.

Using molecular techniques, strains of rabies occurring in bats can be distinguished from those in other mammals. Human deaths from bat strains of rabies have been reported in the New World (27 cases in the United States and Canada between 1980 and 2000) and in Europe. In Australia, at least one human death was caused by another lyssavirus reported from bats. Biting appears to be the main route of infection, and strains of bat rabies have been found in other mammals. People bitten by bats should obtain post-exposure rabies vaccinations as soon as possible after the incident.

Images of bats abound in some human cultures, from depictions in Chinese art, on military emblems, and on coats of-arms. Bats may be positive or negative symbols, but often people do not know what they represent. It is obvious that at least some people have a long fascination with bats.

In China, the "wu fu" (five bats) is commonly portrayed on dishes and robes. In this case, the bats are arranged in a circle facing inward and they depict the five blessings: good health, long life, wealth, love of virtue, and a peaceful death. Chinese bats are often shown in red, the color of joy, and they may carry other positive symbols such as blossoms or fruit. Bats carrying swastikas are jarring images for those unfamiliar with the underlying symbolism. In some Chinese dialects, the word for swastika sounds the same as the word for 10,000. The bat image symbolizes a blessing, but the swastika image it carries turns it into 10,000 blessings.

The Maya god of the underworld, Zotz has the head of a vampire bat on a human body. Zotz usually carries a bleeding heart. Other Mayan portrayals of bats reflect knowledge of different species, from leaf-nosed bats (family Phyllostomidae) to ghost-faced bats (genus Mormoops, family Mormoopidae). The significance of these other bats to the Maya remains unclear, but the Maya unmistakably associated vampire bats with blood and the underworld. Further south in the area that today is northern Colombia and Venezuela, the Taironan people associated vampire bats with human fertility. A woman who had "been bitten by the bat" had started to menstruate. The connection here was to the fertility of women. In some areas of New Guinea, long penises make bats symbols of male fertility.

The connection between bats and blood is strong and recurring, but things are not what they seem in the area of vampires, bats, and blood. In the late nineteenth century, when he was writing Dracula, Bram Stoker wrote bats into the book, perhaps because blood-feeding bats were in the news. European explorers and naturalists had long been intrigued by blood-feeding bats and called them vampires. Indeed, many bats that eat fruit or animals are called vampyressa, vampyrops, or vampyrum, reflecting this fascination. In Africa, India, Southeast Asia, and Australia, there are false vampire bats.

In human folklore, vampires are people who come back from the dead to feed on the blood of living people. Folklore about vampires is widespread in parts of the world where it typically has nothing to do with bats. Vampire bats occur only in the New World tropics (parts of Central and South America). For Europeans, the name vampire goes from human folklore to the bat, not the other way around. Vampire bats, the blood-feeders, do not occur in Transylvania, Africa, India, or Australia.

Modern military units with bats on their emblems are often those associated with electronic warfare. The parallel is with bats and echolocation (or biosonar). At least one British unit has a tiger moth on its emblem, reflecting the defensive behavior of these moths: some tiger moths use acoustic signals to thwart the attacks of bats. The most famous bat in the world, the Bacardi bat, also has a military connection. This bat comes from Spain where it was associated with a victory of the Spanish over the Moors. On the eve of the battle, the bat that flew into the tent of James I of Aragon proved to be a good omen. The bat was then placed on the city of Valencia's coat of arms. This story trail ends up with a bat symbol on a bottle of rum.

But most of the 1,000 or so species of bats have little to do with people and vice versa. A few fruit-eating bats impact economically as pests of commercial crops, and vampire bats may be responsible for spreading rabies among livestock. On balance, other bats pollinate plants that are ecologically (and sometimes economically) important, while still others disperse seeds and play a vital role in reforestation. Insect-eating bats consume vast quantities of insects every year, including some agricultural pests.

Although bats are occasionally harvested as human food, and may be important economically as pollinators or agents of reforestation, they are rarely exploited economically. One important exception is the harvesting of bat guano, an activity that may disturb bats. In many parts of the world, there is a long tradition of harvesting bat guano for fertilizer. Today in Canada, some garden stores sell bat guano from the Philippines. In the past, bat guano has been a source of saltpeter for gunpowder. During the War of 1812, American forces depended upon bat guano for some of their gunpowder. Later, during the Civil War in the United States, Confederate forces were likewise partly dependent upon bats.

Resources

Books

Allen, G. M. Bats. Cambridge: Harvard University Press, 1939

Altringham, J. D. Bats: Biology and Behaviour. London: Oxford University Press, 1996.

Barber, P. Vampires, Burial, and Death: Folklore and Reality. New Haven: Yale University Press, 1998.

Bates, P. J. J., and D. L. Harrison. Bats of the Indian Subcontinent, Sevenoaks, England: Harrison Zoological Museum, 1997.

Bonaccorso, F. J. Bats of Papua New Guinea. Washington: Conservation International, 1998.

Brosset, A. La Biologie des Cchiroptères. Paris: Masson et Cie, 1966.

Fenton, M. B. Communication in the Chiroptera. Bloomington: Indiana University Press, 1985.

——. Bats: Revised Edition. New York: Facts On File Inc., 2001.

Findley, J. S. Bats: A Community Perspective. Cambridge: Cambridge University Press, 1993.

Fleming, T. H., and A. Valiente-Banuet, eds. Columnar Cacti and Their Mutualists. Tucson: University of Arizona Press, 2002.

Greenhall, A. M., and U. Schmidt, eds. The Natural History of Vampire Bats. Boca Raton: CRC Press, 1988.

Griffin, D. R. Listening in the Dark. New Haven: Yale University Press, 1958.

Hill, J. E., and J. D. Smith. Bats: A Natural History. London: British Museum of Natural History, 1984.

Hutson, A. M., S. P. Mickelburgh, and P. A. Racey. Microchiropteran Bats—Global Status Survey and Conservation Action Plan. Gland, Switzerland: IUCN, 2001.

Jackson, A. C., and W. H. Wunner, eds. Rabies. New York: Academic Press, 2002.

Kunz, T. H., ed. Ecology of Bats. New York: Plenum Press, 1982.

Kunz, T. H., and M. B. Fenton, eds. Bat Ecology. Chicago: University of Chicago Press, 2003.

Marshall, A. G. The Ecology of Ectoparasitic Insects. London: Academic Press, 1981.

Neuweiler, G. Biology of Bats. Oxford: Oxford University Press, 2000.

Norberg, U. M. Vertebrate Flight, Mechanics, Physiology, Morphology, Ecology and Evolution. Berlin: Springer-Verlag, 1989.

Nowak, R. M. Walker's Mammals of the World, 6th edition. Baltimore: Johns Hopkins Press, 1999.

Popper, A. N., and R. R. Fay, eds. Hearing by Bats. New York: Springer-Verlag, 1995.

Ransome, R. D. The Natural History of Hibernating Bats. London: Christopher Helm, 1990.

Reid, F. A. A Field Guide to the Mammals of Central America and Southeast Mexico. New York: Oxford University Press, 1997.

Roeder, K. D. Nerve Cells and Insect Behavior, Revised Edition. Cambridge: Harvard University Press, 1967.

Schober, W., and E. Grimmberger. The Bats of Europe and North America. Neptune City, FL: TFH Publications Inc., 1997.

Taylor, P. J. Bats of Southern Africa. Pietermaritzberg, South Africa: University of Natal Press, 2000.

Tupinier, D. La Chauve-souris et l'Homme. Paris: Editions L'Harmattan, 1989.

Tuttle, M. D. America's Neighborhood Bats. Austin: University of Texas Press, 1988.

Wimsatt, W. A., ed. Biology of Bats, Volume 1. New York: Academic Press, 1970.

——, ed. Biology of Bats, Volume 2. New York: Academic Press, 1970.

——, ed. Biology of Bats, Volume 3. New York: Academic Press, 1977.

Periodicals

Simmons, N. B., and J. H. Geisler. "Phylogenetic Relationships of Icaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx with Comments on the Evolution of Echolocation and Foraging Strategies in Microchiroptera." Bulletin of the American Museum of Natural History 235 (1998): 1–182.

Melville Brockett Fenton, PhD