Horseshoe bats
(Rhinolophidae)
Class: Mammalia
Order: Chiroptera
Suborder: Microchiroptera
Family: Rhinolophidae
Thumbnail description
Small to medium-sized, insectivorous bats with complex, horseshoe-shaped noseleaf, large, pointed ears, broad, rounded wings, and short tail enclosed within the flight membrane
Size
Head and body length 1.4–4.3 in (3.5–11 cm); tail 0.6–2.2 in (1.5–5.6 cm); forearm 1.2–3 in (3–7.5 cm); weight 0.15–13.8 oz (4–35 g)
Number of genera, species
1 genus; up to 70 species
Habitat
Open, scrub, savanna, woodland, or forested habitats with roosting sites (caves, rock outcrops, tunnels, mines, or buildings) at low to high altitudes in tropical and temperate zones
Conservation status
Critically Endangered: 1 species; Endangered: 2 species; Vulnerable: 8 species; Lower Risk/Near Threatened: 20 species; Data Deficient: 7 species
Distribution
Throughout tropical and temperate regions of the Old World, from western Europe and Africa through Asia to Japan, Australia, and western Pacific islands
Evolution and systematics
The horseshoe bats (Rhinolophidae) are included here in the superfamily Rhinolophoidea with the Old World leaf-nosed bats (Hipposideridae). However, many authorities believe there is strong evidence that the two groups are sister taxa and recognize them as subfamilies within the Rhinolophidae.
Up to 70 species are recognized within the single genus Rhinolophus. The most recent classification (Nowak 1999) lists 62 species separated into 12 groups.
Fossil Rhinolophidae are known from the early to middle Eocene and early Oligocene of Europe, the Miocene of Australia and the Miocene and late Pliocene deposits of Africa. In 1992, Bogdanowicz and Owen suggested that the family originated in Southeast Asia, that the megaphyllus group includes the most primitive species and that the Palearctic and African species are generally the most advanced.
Physical characteristics
Horseshoe bats are characterized by a complex noseleaf expansion of the skin surrounding the nostrils and consisting of three parts. The horseshoe-shaped lower part covers the upper lip, surrounds the nostrils, and has a central notch in the lower edge. Above the nostrils is the lancet, a pointed, erect structure attached by its base. The horseshoe and the lancet are flattened from front to back. The sella is located between the horseshoe and the lancet, is flattened from side to side and is connected at its base by means of folds and ridges. The form of the noseleaf is often diagnostic in species identification. Horseshoe bats generally fly with the mouth closed and emit ultrasonic sounds through the nostrils. The sounds are channeled by the noseleaf structure to achieve a maximum intensity at a point of focus ahead of the bat, and the noseleaf also shields the ears from the direct reception of the impulses. In some species, such as Hildebrandt's horseshoe bat (R. hildebrandti), the noseleaf has a distinctly arranged pattern of sensory hairs.
The large ears are widely separated, usually pointed, and lack a tragus, but the antitragal lobe is much enlarged and folds across the open base of the ear. The ears are capable of independent movement. The eyes are quite small, and the field of vision seems to be partly obstructed by the noseleaf, so sight is probably of little importance.
The fur of horseshoe bats is long, loose, and soft. The most common colors are gray-brown to rufous-brown, but the color varies from black or dark brown to bright orange-red or cream-yellow. The underparts are usually more pale than the upperparts. The woolly (R. luctus) and lesser woolly (R. beddomei) horseshoe bats have a very long, woolly pelage, unusual in the genus.
The wings are short, broad, and rounded, the second finger consisting of the metacarpal only, without phalanges. The third, fourth and fifth fingers each have two phalanges, which fold under the wing when the bat is at rest. The vertebrae of the tail end at the posterior fringe of the interfemoral membrane, which is supported on either side by curved calcanea arising from the ankles. The tail and interfemoral membrane fold upwards when the bat is resting. The hind limbs are poorly developed and these bats cannot walk quadrupedally. All the toes have three bones, except the first, which has two; the Hipposideridae, in contrast, have only two bones in each toe.
Females have two mammary glands in the pectoral region and two "false nipples" on the lower abdomen, just anterior to the genital orifice, to which the young cling while they are carried around by their mother during flight. In two African species, the small Lander's horseshoe bat and the larger R. alcyone, the males have glandular hair tufts in the armpit area that are noticeable by their coloring. These males also have well-developed nipples, which do not produce milk, but perhaps secrete odor-producing substances.
Young horseshoe bats shed milk teeth before birth. The teeth of adults exhibit the normal cuspidate pattern found in insectivorous bats. The dental formula is: (I1/2, C1/1, PM2/3, M3/3) × 2 = 32. The upper incisors are mounted in a projection of the palatine bone, well forward of the canines. The lower incisors are trifid. The first upper and second lower premolars are small, usually displaced externally, and may be missing. The most characteristic feature of the skull is the dome just above the nasal aperture.
Distribution
Horseshoe bats occur throughout the temperate and tropical zones of the Old World, from the British Isles across southern and central Europe, through Arabia and southern Asia, east to China and Japan, and throughout the Indian subcontinent, Southeast Asia, Indonesia, and the Philippines to Australasia and western Pacific islands. They also occur throughout Africa, except in the most arid regions, but not in Madagascar. The most wide-ranging species is the greater horseshoe bat (R. ferrumequinum), which occurs through the entire southern Palaearctic region from Great Britain across Europe, North Africa, and southern Asia east to China and Japan. In contrast, some island species have very restricted ranges. For example, the Andaman horseshoe bat (R. cognatus) is confined to three known areas on the Andaman Islands in the Indian Ocean, while R. monoceros occurs only on Taiwan and R. imaizumii only on Iriomote Island in the southern Ryukyu Islands, south of Japan. A few continental species also have very small ranges. The mitred horseshoe bat (R. mitratus) is known from only one specimen collected in Bihar, eastern India, while R. paradoxolophus is known by only single specimens from northern Vietnam and eastern Thailand, and in Africa the Cape horseshoe bat (R. capensis) is endemic to South Africa and R. maclaudi is confined to Guinea in West Africa.
Habitat
The Rhinolophidae occur throughout the temperate and tropical zones of the Old World, being found in a great variety of habitats at both high and low altitudes. They are found in forest, woodland, savanna, scrub, open areas, and sometimes even in deserts, but it seems that the availability of suitable shelters for daytime roosting, nurseries, and hibernation is often a more important factor governing habitat suitability than is the type of vegetation occurring in the occupied area. The variety of sites used for such shelters is extensive, and includes caves, rock outcrops and crevices, overhangs, mines, tunnels, buildings (disused and occupied), cellars, culverts, hollow trees, and dense foliage. Hildebrandt's horseshoe bat of eastern Africa even uses disused aardvark (Orycteropus afer) and warthog (Phacochoerus aethiopicus) holes for daytime roosts, but also roosts in hollow trees, especially the baobab (Adansonia digitata), and buildings.
Forest-inhabiting species include the rufous horseshoe bat (R. rouxii), whose diurnal roosts tend to be humid and include caves, tunnels, hollow trees, wells, temples, old houses, and barns. The little-known little Nepalese horseshoe bat (R. subbadius) is recorded from bamboo clumps in dense jungle. Although Blyth's horseshoe bat (R. lepidus) is normally associated with forested country, it is also recorded from a desert biome in India; its diurnal roosts include subterranean silos. The woolly horseshoe bat occurs in dense forests on precipitous mountains in the Kathmandu Valley, where it roosts in caves. The lesser woolly horseshoe bat is also restricted to forest, where it roosts in hollow trees, small caves, and under ledges; it also uses dungeons, old houses, barracks, and tunnels. The trefoil horseshoe bat (R. trifoliatus) of southern, southeastern Asia and Malaysia lives in dense evergreen jungle and roosts in thick foliage. Lander's horseshoe bat (R. landeri) of Africa is predominantly a forest species but in the south of its range it inhabits savanna woodland with riverine vegetation and well-watered areas. The presence of substantial shelters (caves, mines, boulders, hollow trees) is probably a critical habitat requirement.
The African endemic Ruppell's horseshoe bat (R. fumigatus) is widespread in African open savanna woodland but is absent from desert and semidesert areas. In contrast, Geoffroy's horseshoe bat (R. clivosus), which occurs in Africa and Asia, inhabits savanna woodland but also occurs in deserts. In southern Africa its absence from semidesert parts of Botswana may be due to the lack of suitable roosting sites such as caves, rock crevices, and mines. The bushveld horseshoe bat (R. simulator) of African savanna woodland is dependent on the availability of caves and mine shafts for shelter.
Some horseshoe bat species occur in association with man. The greater horseshoe bat uses caves but has adapted to larger buildings for nurseries, especially in the northern parts of its European range, while in southern Asia it roosts in temples, outhouses, and ruins. Also in Europe, the nurseries of the lesser horseshoe bat are predominantly in warm caves on southern regions, but mostly in roofs of buildings in the north. This species hibernates in caves, mines, and cellars.
Behavior
Roosting habits within the family are diverse. Most species are predominantly cave dwellers, but some have adapted to human-made structures such as mines and buildings (see Habitat section). Historically, in Europe the lesser horseshoe bat roosted all year round in caves, but it has changed its behavior markedly and has adopted buildings as summer roosts in many areas. Most species are gregarious, roosting in small to large colonies, but the woolly horseshoe bat normally lives in pairs. Some species, such as the greater, rufous big-eared (R. macrotis), intermediate (R. affinis) and Blyth's, may roost together. Blyth's and intermediate may roost with bats from other genera (Hipposideros, Rhinopoma, Taphozous). In some species the sexes live together all year, whereas in others, such as the greater horseshoe bat, the females form single-sex maternity colonies. Eastern horseshoe bat (R. megaphyllus) colonies are usually small (fewer than 20 individuals), but in the nonbreeding season may reach 2,000 individuals, while in South Africa, Geoffroy's horseshoe bat occurs in roosts of up to 10,000 individuals.
When resting, the bats hang freely from the ceiling of the cave or other shelter, some species with individuals well separated and others with individuals close together. They do not close their wings alongside their body as do most bats, but wrap them wholly or partially around the body. The small bare patch on the back at the base of the tail is covered by the upturned tail and membrane, so that the bat is enclosed in its flight membranes.
Those species that live in temperate zones hibernate during the cold season, although they interrupt their hibernation from time to time and may change their hibernating places occasionally. Species such as the eastern horseshoe bat, which occupy both tropical and temperate zones, remain active throughout the year in the tropical parts of their range. Most hibernating species leave their daytime roosts at the end of the summer and seek alternative winter hibernation sites (hibernacula) in more sheltered situations. Some species commonly move over distances of 3.1–6.2 mi (5–10 km) between summer and winter sites. Greater horseshoe bats often start hibernating near the entrance of caves, then move to sites deeper in the caves as the temperature drops and winter advances. Most species hibernate colonially but some (such as the eastern horseshoe bat) hibernate singly. Hibernacula are often humid, usually have an ambient temperature of around 42.7–50°F (6–10°C) (measured in Europe), and have restricted airflow. Close access to sheltered winter foraging areas is important, as is freedom from disturbance. Daily torpor is also common in horseshoe bat species in response to cooling and/or reduced food availability. In summer, torpor is slight and bats can fly off quickly.
Feeding ecology and diet
Horseshoe bats are aerial foragers, catching flying prey on the wing, and some are also gleaners, snatching stationary prey from branches, foliage, stones, or the ground. Many are clutter foragers, using their broad, short wings and high echolocation frequencies to fly slowly and maneuver through dense vegetation. Many species also "flycatch" or "perch-hunt" by hanging from a perch and making rapid sallies to snatch prey detected flying past. Some species can hover. Horseshoe bats usually hunt within 16.5–19.5 ft (5–6 m) of the ground, and will also feed on the ground. Prey can be caught in the wing membrane and may be stored for brief intervals in cheek pouches. The relatively short tail and small tail membrane are not large enough to form a pouch for holding insects. When a large insect is caught in flight, it may be tucked into the wing membrane under the arm while the bat manipulates it with its mouth.
Horseshoe bats begin foraging later in the evening than most bats and often return to the roost, or to a feeding perch, to eat captured prey. Such perches can often be located by the piles of insect fragments that collect on the ground beneath them. In general Rhinolophus species are solitary hunters, while Hipposideros species forage in small groups. Like many other bats, horseshoe bats generally have regular feeding territories or hunting areas, and greater horseshoe bats may hunt regularly around the periphery of the same trees, low bushes, and buildings. Blyth's horseshoe bats have small, well-defined foraging territories near their roosts. They explore the foliage of trees, making frequent stops to pick insects off leaves. Some species are attracted to insects flying around lights and may enter buildings in search of prey. Hildebrandt's horseshoe bat hunts on the wing during the early part of the night, after which it flycatches throughout the night. The rufous horseshoe bat adopts a similar feeding strategy. The greater horseshoe bat changes its foraging habitat seasonally, hunting in woodland in the spring and over pasture in late summer. This behavior is linked to prey availability: the ambient temperature in woodlands is higher than that over open ground, leading to higher insect numbers in spring, while Aphodius dung beetles, a favored prey, increase in pasture during the summer as cattle dung accumulates.
Echolocation pulses are emitted through the nostrils with the mouth closed. The echolocation calls are of high duty cycle (56–60%), are of constant frequency with a short frequency drop at the end, and are often exceptionally long (20 to over 100 ms) in duration. To a certain extent, frequency can be used to identify a species, since individual species emit signals over a characteristic limited frequency band. Signal intensity (loudness) 4 in (10 cm) in front of the bat has been recorded at 27.0 N/m2 in the greater horseshoe bat and 2.0 N/m2 in the Mediterranean horseshoe bat R. euryale. The former species can differentiate between two identical targets, one placed as little as 0.47–0.51 in (12–13 mm) in front of the other, while the latter can detect a 0.12 in (3 mm) wire at a range of 4.6 ft (1.4 m) and a 0.002 in (0.05 mm) wire at 8 in (20 cm).
Prey items include Lepidoptera (almost entirely moths, including microlepidoptera), Coleoptera (including cockchafers and dung beetles), Hemiptera, Diptera (including mosquitoes and craneflies), Orthoptera (grasshoppers), Hymenoptera (wasps), Isoptera (termites), and spiders. The greater horseshoe bat drinks during low-level flight or while hovering.
Reproductive biology
Courtship and mating behavior are poorly known, but lesser horseshoe bats chase each other as a preliminary to mating, the male then hanging himself behind and over the female for the very brief copulation. Polygyny may be common, a male mating with a harem of females. In some species, dominant males guard favored mating caves, and in Britain individual greater horseshoe bats are known to guard the same spot at cave entrances for a large number of years, and to be visited by a number of females during the mating period. The existence of strictly monogamous family units in any species has not been proved, but the woolly horseshoe bat apparently lives in pairs—whether these pairs are permanent is not clear.
In some species, including those that hibernate, mating occurs during the autumn, and may continue during the winter, but ovulation is delayed so that fertilization does not occur until the spring. In other species mating and fertilization occur in the spring, and in tropical regions births usually take place during the warm, wet months. In South Africa, Geoffroy's horseshoe bat copulates in May, at the end of the summer, and sperm are stored in the female's oviducts and uterine horns during winter hibernation. Ovulation and fertilization take place in spring (August) and parturition in December. In the cape horseshoe bat, sperm storage devolves upon the male. Spermatogenesis takes place in October–May and sperm are released to the cauda epididymis in April–May. At this time, females are in estrus, but copulation and ovulation are delayed until August–September, after the winter hibernation. Male eastern horseshoe bats of Australia undergo spermato-genesis in February, produce mature sperm in March, and store the sperm until mating, ovulation and fertilization take place in June.
Gestation periods vary from 7 weeks to 3–4.5 months, reaching over 5 months in the rufous horseshoe bat in India. A single young is normally produced, but in India the greater horseshoe bat apparently regularly gives birth to twins. Birth weight is around 0.07–0.2 oz (2–6 g) and lactation continues for 1–3 months. Young are independent at 6–8 weeks. After weaning, the young are usually abandoned by the mothers, but may stay at the breeding site for some time afterwards. Females of some species become sexually mature in their first year, males often not until the second year. In some species, sexual maturity is delayed: male greater horseshoe bats mature at 3 years (but often do not acquire a territory for another 1–2 years) and females at 3–4 years. One breeding season appears to be the norm, but in Malaysia the intermediate horseshoe bat apparently breeds twice a year, with pregnant females collected in April–May and again in October. Longevity in the genus is typically 4–7 years, but there are several records of much longer lifespans. The record is that of a greater horseshoe bat that was captured in France in 1982, 29 years after initial banding, and was then seen again in 1983. In this species, most mortality occurs in the first winter, or when females first breed.
Conservation status
Many horseshoe bat species are poorly known and their conservation status is therefore difficult to assess. However, all the species are vulnerable to loss of foraging habitat through destruction or modification, while they are also (and more significantly) threatened by the loss of roost sites, nurseries, and hibernacula as a result of destruction, disturbance, or vandalism. The widespread use of insecticides is also a threat to some species. The IUCN Red List contains 38 species, 57% of the total species in the family, including 7 that are Data Deficient and 20 that are Lower Risk/Near Threatened. The only Critically Endangered species is the recently described R. convexus of Malaysia. The two Endangered species both have a very restricted island distribution, the Kai horseshoe bat (R. keyensis) being confined to the Kai Islands (Indonesia), and R. imaizumii being restricted to one island in the Ryukyu group south of Japan. The Vulnerable Andaman horseshoe bat also has a restricted island distribution and a small, possibly declining population.
Although the survival of the more widespread species may not be of serious concern globally, regionally the situation may well be more serious. For example, the greater horseshoe bat is globally classed as Lower Risk/Near Threatened but is regarded as endangered in Europe, where it is threatened with extinction in northern parts of its range. It is declining rapidly as a result of disturbance to its roosts in caves and buildings, vandalism, habitat modifications leading to the loss of large insect prey, and the increasing use of insecticides. Similar problems have beset the lesser horseshoe bat, which is already extinct in northern central Europe and northern Britain, and is threatened with extinction in Germany. This species, with Blasius's (R. blasii), Mediterranean (R. euryale), and Mehely's (R. mehelyi) horseshoe bats, have also been listed as endangered in Europe. A slow recovery of the Mediterranean horseshoe bat has been noted since the most dangerous pesticides were banned in the 1980s, while in Britain the decline of the greater horseshoe bat has been halted by protecting maternity roosts and hibernacula.
The 18 horseshoe bat species that occur in the Philippines are poorly studied there but are known to have been impacted by the widespread disturbance of caves. Other species roost in large hollow trees, especially in lowland dipterocarp forest, and have been severely affected by logging that destroys both the roosting trees and the foraging habitat.
Significance to humans
The folklore, superstitions, and legends that surround bats in general also apply to the Rhinolophidae, but without any specific reference to any species in this family. Horseshoe bats have no significance to humans in terms of public health, or nuisance factors, and relatively few species roost extensively in human-made structures such as occupied buildings.
Species accounts
Eastern horseshoe batRufous horseshoe bat
Lesser woolly horseshoe bat
Greater horseshoe bat
Cape horseshoe bat
Dent's horseshoe bat
Blasius's horseshoe bat
Mediterranean horseshoe bat
Lesser horseshoe bat
Resources
Books:Bates, P. J., and D. L. Harrison. Bats of the Indian Subcontinent. Sevenoaks, UK: Harrison Zoological Museum, 1997.
Churchill, S. Australian Bats. Sydney: Reed New Holland, 1998.
Corbett, G. B., and J. E. Hill. The Mammals of the Indomalaysian Region. Oxford: Oxford University Press, 1992.
Hill, J. E., and J. D. Smith. Bats: A Natural History. London: British Museum (Natural History), 1984.
Koopman, K. F. "Order Chiroptera." In Mammal Species of the World, edited by D. E. Wilson and D. M. Reeder. Washington, DC: Smithsonian Institution Press, 1983.
Kunz, T. H., and P. A. Racey, eds. Bat Biology and Conservation. Washington, DC: Smithsonian Institution Press, 1998.
Nowak, Ronald M. Walker's Mammals of the World. 6th ed. Baltimore: The Johns Hopkins University Press, 1999.
Schober, W., and E. Grimmberger. Bats of Britain and Europe. London: Hamlyn, 1993.
Skinner, R., and R. H. N. Smithers. The Mammals of the Southern African Subregion. 2nd ed. Pretoria, South Africa: University of Pretoria, 1998.
Periodicals:Bogdanowicz, W., and R. D. Owen. "Phylogenetic Analyses of the Bat Family Rhinolophidae." Zeitschrift für zoologische Systematik und Evolutionsforschung 30 (1992): 142–160.
Organizations:Australian Museum. 6 College Street, Sydney, New South Wales 2010 Australia. Phone: (2) 9320 6000. Web site:
Bat Conservation International. P.O. Box 162603, Austin, TX 78716 USA. Phone: (512) 327-9721. Fax: (512) 327-9724. E-mail: batinfo@batcon.org Web site:
Eurobats. Martin-Luther-King Str. 8, Bonn, D-53175 Germany. E-mail: eurobats@uno.de Web site:
IUCN Species Survival Commission, Chiroptera Specialist Group. Web site:
[Article by: Barry Taylor, PhD]
