Heterohyrax brucei (J.E.Gray, 1868)

Don E. Wilson & Russell A. Mittermeier, 2011, Procaviidae, Handbook of the Mammals of the World – Volume 2 Hoofed Mammals, Barcelona: Lynx Edicions, pp. 41-47 : 45-46

2.

Bush Hyrax

Heterohyrax brucei

French: Daman de Bruce / German: Buschschliefer / Spanish: Daman de arbustos

Other common names: Yellow-spotted Hyrax

Taxonomy. Hyrax brucei: Gray, 1868 ,

Ethiopia (= Abyssinia).

Various names have been applied to the Bush Hyrax including Dendrohyrax blainvillii , Heterohyrax blainvillii , Hyrax syriacus and even Procavia brucei . Many different subspecies have been described from Africa, and two forms, antineae and chapini, have been considered distinct species. However, H. antineae , reported for the Ahaggar Mountains in Algeria is incorrect, as there only the Rock Hyrax ( P. capensis ) occurs. H. chapini from Matadi in east-central DR Congo, supposedly characterized by the presence of only two pairs of inguinal teats, is included here as a subspecies of the Bush Hyrax. Although no consensus exists on whether all of these subspecies are conspecific, sequences of the mtDNA cytochrome b gene indicate that at least subspecies hindei in the central portion of the range and subspecies ruddi and grant: from Zimbabwe and South Africa are highly distinct and may represent cryptic species. Further genetic studies over the whole range are necessary to determine the taxonomy of the Bush Hyrax. The chromosome number is 2n = 54. The karyotype is marked by 20 acrocentric, two subtelocentric, two submetacentric, and two metacentric autosomal pairs. The X chromosome is the largest submetacentric and the Y is a very small acrocentric. Substantial geographic variation in coat color has been recorded from across the range of this species, and has led to a proliferation of described forms. No fewer than 34 synonyms are known, many of which have been considered subspecies by some authors. Twenty-four subspecies presently recognized.

Subspecies and Distribution.

H.b.bruceiGray,1868—Ethiopia.

H.b.albipesHollister,1922—Kenya.

H.b.bakeriGray,1874—Uganda.

H.b.bocageiGray,1869—Angola.

H.b.chapiniHatt,1933—DRCongo.

H.b.dieseneriBrauer,1917—Tanzania.

H.b.fromm:Brauer,1913—Tanzania.

H.b.grantiWroughton,1910—SouthAfrica.

H.b.hindeiWroughton,1910—Kenya.

H.b.hoogstraaliSetzer,1956—Sudan.

H.b.kemp:Thomas,1910—Kenya.

H.b.lademanniBrauer,1917—Tanzania.

H.b.manningiWroughton,1910—Malawi.

H.b.mossambicusPeters,1870—Mozambique.

H.b.muenzneriBrauer,1913—Tanzania.

H.b.princepsThomas,1910—Ethiopia.

H.b.prittwitziBrauer,1917—Tanzania.

H.b.pumilusThomas,1910—Somaliland.

H.b.rudd:Wroughton,1910—Mozambique.

H.b.rudolfiThomas,1910—Ethiopia.

H.b.somalicusThomas,1892—Somaliland.

H.b.ssongeaeBrauer,1917—Tanzania.

H.b.thomasiNeumann,1901—Sudan.

H. b. victorianjansae Brauer, 1917 — Tanzania.

Endemic to Africa from NE Sudan throughout the Horn of Africa, south to Limpopo and Mpumalanga provinces in South Africa, and also isolated populations in Angola. Determining the limits of subspecific distribution is not possible for the moment, but the subspecies and the countries bearing their type localities are included above.

Descriptive notes. Head-body 32-56 cm; weight 1.3-3. 6 kg. Small to medium-sized, with short legs, rudimentary tail, round ears, and rabbit-like appearance. Males and females are, on average, of similar size, although females are sometimes larger than males. Lateral and dorsal color varies from gray to dark reddish-brown. Some individuals in isolated populations can be white-spotted. Usually a small, linear, creamy to yellow spot in the mid-line of the back surrounds the dorsal gland, but in some subspecies it may be lacking. Ventral color is white or creamy, in distinct contrast to the sides, back, head, and rump. Eyebrows are strikingly white to creamy and conspicuous at a distance. Vibrissae (up to 90 mm long on the snout) are evident on the snout, above the eyes, under the chin, along the back and sides, on the abdomen, and on foreand hindlimbs. These hairs provide tactile feedback to the animals when they are in the dark holes and crevices where they hide and rest. The ears are more prominent than in other hyraxes, the eyes bulge, and the head is flat dorsally. Guard hairs are blacktipped, and up to 30 mm long. The underhairs are brown or gray at the base. The anal-preputial mean distance in males is 6:5.8-2 cm, two or three times that of other genera. Anatomy of the penis is complex; it is round in cross section, with an appendage at the tip, and measures greater than 6 cm when fully erect. Femalestypically have one pair of pectoral and two pairs of inguinal mammae, though in some individuals the pectoral pair is absent. A dorsal gland lies beneath a raised patch of skin approximately 1-5 cm long. In adults the gland is surrounded by erectile hairs. The lobules in the glands of mature, sexually active adults are made up of 25-40 alveoli of secreting epithelium surrounding a lumen. The gland is odiferous and may function in mating and recognition of the mother by young. During courtship the male erects the hairs of the dorsal spot, exposing the dorsal gland. Hair erection of the dorsal spot also functions as an alarm or threat signal to hyraxes and other nearby animals. Bush Hyraxes have a single pair of tusk-like upper incisors. These are ridged or triangular in cross section in males; the faces of these incisors are rounded in females. A gap (diastema) 10-16 mm long separates the incisors from the premolars in adults. Premolars and molars are brachydont (short crowns and relatively long roots) adapted for a herbivorous diet. The length of the upper premolar toothrow, P'~* is just less than or equal to that of the upper molar toothrow, M'-*. As with all hyraxes, the digits have flat, hoof-like nails, except for the inner toe of the hindfoot, which has a long, curved claw for grooming; in addition, the four lower incisors are comb-like for grooming the fur. The soles have thick, rubbery pads with numerous skin glands that increase the grip for climbing. Bush Hyraxes are agile in climbing and jumping among branches. The weight-specific metabolic rate is low, with a thermo neutral zone of 24-35°C. Body temperature typically ranges from 35°C to 37°C, but fluctuates up to 7°C with air temperature. At air temperatures above 25°C body temperature is maintained by evaporative water loss from the nostrils, soles of the feet, panting, salivating, and grooming. Wateris conserved by low urine and fecal volume and highly concentrated urine that, together with feces, forms a dark, crystalline residue called hyraceum at communal latrines. Most water is obtained from browsing material; free water is seldom consumed, because of low metabolic rate, low urine volume, and thermallability. Behavioral thermoregulation is achieved by early morning and late afternoon basking on the surface and retreating to rock crevices and shaded areas in midday to avoid heat and dehydration. Individuals conserve heat by huddling and stacking.

Habitat. Restricted to rocky outcrops (kopjes) and piles of large boulders with openings at least 11 cm in height and with 1 m * of floor space. Rock crevices provide a constant, moderate temperature (17-25°C) and humidity (32-40%) and protection from fire. Bush Hyraxes are sometimes found living in the holes offig trees near rivers. In East Africa, they live at elevations up to 3800 m. Bush Hyraxes are frequently found in the company of Rock Hyraxes, sometimes even inhabiting the same rock crevices. This heterospecific association varies seasonally in Zimbabwe, but is especially evident during synchronous parturition in March. They are often conspicuous and common in appropriate habitat. Densities in Matobo National Park in Zimbabwe ranged from 0-51 ind/ha to 1:92 ind/ha. In the Serengeti, densities reached 75 ind/ha in kopjes where only Bush Hyraxes were found and 28 ind/ha where they were sympatric with Rock Hyraxes. Rainfall, through its effect on fecundity, appears to be the primary factor responsible for annual fluctuations in abundance. The principal predator is Verreaux’s eagle (Aquila verreauxii); Bush Hyraxes and Rock Hyraxes make up more than 90% of this eagle’s diet. In Zimbabwe, Verreaux’s eagles selected adults disproportionately. Other predators include large snakes, Leopards (Panthera pardus), martial eagles (Polemaetus bellicosus), and other raptors. Bush Hyraxes are susceptible to viral pneumonia and tuberculosis. The sarcoptic mite that causes mange can heavily reduce colonies. Individuals can harbor the flagellate Leishmania, and nematode Crossophorus collarus. Ectoparasites collected from live-captured individuals in Zimbabwe included ixodid ticks (Rhipicephalus distinctus and Haemaphysalis leachit), fleas (Procaviopsylla), lice (Prolignognathus), and ear mites (Acomatacarus). Individuals often dust-bathe to remove ectoparasites.

Food and Feeding. Bush Hyraxes are obligate browsers, spending more than 80% of their foraging time browsing on twigs and bark of woody species and leaves, buds, flowers, and fruits of trees, bushes, and forbs; they rarely consume grass. The feeding preference for a particular species is greatly influenced by the optimal location of the plant, on the one hand, and its stage of development, on the other; young leaves, flowers, and fruit are much relished. Preferred plant species are regularly and systematically cropped by members of a family group until very little edible material is left. The animals then move to another part of the home range and continue browsing there from preferred bushes and trees. While the members of the group are feeding, the territorial male will usually stand guard on a high rock or tree branch and be the first to call in a case of danger. In the Serengeti, Bush Hyraxes were observed feeding on 64 plant species. The most commonly foraged plants were Acacia tortilis, Allophylus rubifolius, Cordia ovalis, Grewia fallax, Hibiscus lunarifolius, Ficus glumosa, F. ingens, Iboza sp., and Maerua triphylla. In Zimbabwe the most frequently foraged taxa were Combretum molle, Elephantorrhiza goetzei, Flueggia virosa, Strynchos usambarensis, Kirkia acuminata, Croton gratissimus, Mundulea sericea, Rhus leptodictya, and Commiphora marlothii.

Breeding. Females come into estrus once or twice per year for up to three days, perhaps repeatedly over a four-week period. Estrus in females in a family group is synchronized. Gestation lasts 26-30 weeks. In the Serengeti, two distinct birth seasons, after the long and short rains, were observed. Birth pulses occur in Kenya from February to March,just before the rains, and in Zimbabwe in March, two months after peak rainfall. Litter size averages 1-6 in Tanzania, 1-7 in Kenya, and 2-1 in Zimbabwe. Females may bear young every other year. Young are precocious at birth and weigh 220-230 g. They nurse for 1-5 months and reach sexual maturity at 16-17 months of age. Recorded life span in the wild is more than eleven years in females, similar to records for captivity. Sex ratios ranged from 1:6 to 3:2 females—males in Serengeti. However, in Zimbabwe sex ratios of captured individuals and those that were prey to Verreaux’s eagles did not differ from 1:1. Density of this population was estimated at 0-5-1-1 ind/ ha (1-2-2-6 ind/ha of kopje) overa five-year period. This population comprised 19-4— 27-5% juveniles, 7-2-13-1% subadults, and 62-9-73-7% adults. Juvenile mortality was estimated at 52:4-61-3%.

Activity patterns. Bush Hyraxes are diurnal, with most feeding occurring between 07:30 and 11:00 h and 15:30 and 18:00 h. Individuals may feed alone or in a group. Groups may feed up to 50 m from the center of the colony, although casual feeding rarely occurs more than 20 m from the den site. Feeding bouts average 20 minutes and last no longer than 35 minutes. Individuals can climb vertical trunks of trees and balance on thin branches to strip the vegetation of leaves.

Movements, Home range and Social organization. Bush Hyraxes are gregarious, with group sizes reaching 34 individuals. The social unit is a polygynous harem, with a territorial adult male, up to 17 adult females, and juveniles. Territorial males threaten other males by movements or changes in posture (raising head and shoulders), showing large incisors, grinding molars, growling, snapping, chasing, biting, and erecting hairs around the dorsal gland. Appeasement is communicated with the hair and body flat and rump presented. Latrines, located near sleeping quarters, are visible because of white stains resulting from deposits of urine rich in calcium carbonate. Bush Hyraxes have a highly structured repertoire of calls indicating predator detection, contact, threat, and distress; some of these calls are recognized by Rock Hyraxes and Klipspringers ( Oreotragus spp. ). Loud territorial calls or songs are frequent during the mating season; the territorial call of adult males is shrill and long, lasting about 1-5 seconds, and given repeatedly for up to five minutes. Territorial males copulate more often than peripheral males and mate preferentially with females older than 28 months of age. Peripheral males exhibit a dominance hierarchy and mate more often with young females. The male emits a shrill cry as he approaches to mate, and the female erects her dorsal spot hairs. The male sniffs the female’s vulva,rests his chin on her rump, and then slides onto her back as he makes thrusting movements followed by intromission in 3-5 minutes. A second copulation may occur in 1-3 hours. Mothers suckle only their own young and the young maintain a strict teat order. Young play with conspecifics, and sometimes with young Rock Hyraxes at heterospecific nurseries, by nipping, biting, climbing, pushing, fighting, chasing, and mounting. Young in nurseries are attended by their own mothers, mothers of other young, non-maternal conspecifics, or even female Rock Hyraxes. Femalesjoin the adult female group at sexual maturity (approximately 16 months of age), and male offspring disperse at 12-30 months of age. However, migration of females also has been recorded in the Serengeti. Female migrations prevent inbreeding and are mainly responsible for long-distance gene transfer between kopjes.

Status and Conservation. Currently classified as Least Concern on The IUCN Red Lust. The Bush Hyrax is readily snared. In Zimbabwe and in communal areas and commercial farmlands and unprotected lands elsewhere in southern Africa, they are used to make karosses (blankets), which has resulted in dramatic declines in local population densities. However, overall the species is widespread, and present in several well-managed protected areas across its range.

Bibliography. Ashford (1970), Ashford et al. (1973), Aumann & Chiweshe (1995), Barry (1994), Barry & Barry (1996), Barry & Mundy (1998, 2002), Barry & Shoshani (2000), Bartholomew & Rainy (1971), Bloomer (2009), Bothma (1966, 1971), Caro & Alawi (1985), Coetzee (1966), Crawford-Cabral & Verissimo (2005), De Niro & Epstein (1978), Dobson (1876), Eley (1994), Ellerman et al. (1953), Estes (1991), Fischer (1992), Gargett (1990), Gargett et al. (1995), Gerlach & Hoeck (2001), Glover & Sale (1968), Gray (1868), Grobler & Wilson (1972), Hahn (1934), Hatt (1936), Hoeck (1975, 1977a, 1977b, 1978a, 1978b, 1978c, 1982a, 1982b, 1982c, 1989), Hoeck et al. (1982), Hoffmann et al. (2008), Kingdon (1971, 1997), Leon (1980), Maloiy & Eley (1992), Meesteret al. (1986), Meyer (1978), Prinsloo & Robinson (1992), Roberts (1951), Roche (1962, 1972), Sale (1965a, 1965b, 1966, 1969, 1970a, 1970b), Schlitter (1993), Skinner & Chimimba (2005), Smith (1977), Sokolov & Sale (1981), Thomas (1892), Turner & Watson (1965), Walker et al. (1978), Weigl (2005), Wilson (1969).

Figures

1. Rock Hyrax (Procavia capensis), 2. Bush Hyrax (Heterohyrax brucei), 3. Western Tree Hyrax (Dendrohyrax dorsalis), 4. Southern Tree Hyrax (Dendrohyrax arboreus), 5. Eastern Tree Hyrax (Dendrohyrax validus)

Subspecies and Distribution. H.b.bruceiGray,1868—Ethiopia. H.b.albipesHollister,1922—Kenya. H.b.bakeriGray,1874—Uganda. H.b.bocageiGray,1869—Angola. H.b.chapiniHatt,1933—DRCongo. H.b.dieseneriBrauer,1917—Tanzania. H.b.fromm:Brauer,1913—Tanzania. H.b.grantiWroughton,1910—SouthAfrica. H.b.hindeiWroughton,1910—Kenya. H.b.hoogstraaliSetzer,1956—Sudan. H.b.kemp:Thomas,1910—Kenya. H.b.lademanniBrauer,1917—Tanzania. H.b.manningiWroughton,1910—Malawi. H.b.mossambicusPeters,1870—Mozambique. H.b.muenzneriBrauer,1913—Tanzania. H.b.princepsThomas,1910—Ethiopia. H.b.prittwitziBrauer,1917—Tanzania. H.b.pumilusThomas,1910—Somaliland. H.b.rudd:Wroughton,1910—Mozambique. H.b.rudolfiThomas,1910—Ethiopia. H.b.somalicusThomas,1892—Somaliland. H.b.ssongeaeBrauer,1917—Tanzania. H.b.thomasiNeumann,1901—Sudan. H. b. victorianjansae Brauer, 1917 — Tanzania . Endemic to Africa from NE Sudan throughout the Horn of Africa, south to Limpopo and Mpumalanga provinces in South Africa , and also isolated populations in Angola . Determining the limits of subspecific distribution is not possible for the moment, but the subspecies and the countries bearing their type localities are included above.