Proteles cristata, Sparrman, 1783

Don E. Wilson & Russell A. Mittermeier, 2009, Hyaenidae, Handbook of the Mammals of the World – Volume 1 Carnivores, Barcelona: Lynx Edicions, pp. 234-260 : 252-254

1.

Aardwolf

Proteles cristata

French: Protele / German: Erdwolf / Spanish: Proteles

Taxonomy. Viverra cristata Sparrman, 1783 ,

Eastern Cape Province, South Africa.

Although previously placed in its own family (Protelidae), it is now considered a member of the family Hyaenidae . The Aardwolf belongs to the subfamily Protelinae , of which it is the only extant member. They occur in two distinct populations separated by about 1500 km. However, studies ofthe extent of genetic and morphological differences between these groups have not been conducted. Two subspecies are recognized.

Subspecies and Distribution.

P. c. cristata Sparrman, 1783 — E African coast (S Egypt, Sudan, Eritrea, Djibouti, Ethiopia, Somalia, Kenya, NE Uganda to C Tanzania). P. c. septentrionalis Rothschild, 1902 — most of S Africa (S Angola, S Zambia, SW Mozambique, Namibia, Botswana, Zimbabwe, Swaziland, Lesotho, and South Africa).

Descriptive notes. By far the smallest of the four hyaenid species. Head-body 55-80 cm, tail 20-30 cm, height at shoulder 45-50 cm; weight (adult) 8-12 kg with seasonal variation, and reported as high as 14 kg. No sexual size dimorphism. Superficially similar in appearance to the Striped Hyena, with dark vertical stripes on a buff, yellowish-white or rufous body, and irregular horizontal stripes on the legs. However, the Striped Hyena is more than twice as large with less regular striping. The Aardwolf’s coat is about 2-5 cm long, with longer hairs along the mane and in the bushy tail. The neck is long and the throat is a pale gray-white. The legs are long and slender and the striping terminates in black at the feet. As in the Striped and Brown Hyena, the Aardwolf has long, pointed ears and a long erectile mane extending the length ofits body. Like the other hyaenids, Proteles has a sloping back with the forelegs longer than the hindlegs, and a well-developed anal gland used for scent marking. Females have two pairs of teats. Uniquely among the hyaenids, Profeles has a number of adaptations for feeding exclusively on termites, including a long, spatulate tongue with large and varied papillae, and a large submaxillary gland which produces copious amounts of sticky saliva. Very small peg-like cheek teeth are widely spaced along thejaw margins, yet large canines have been retained for use in territorial disputes with other Aardwolves and defense againstjackals. Their skulls also feature a relatively broad, nearly parallel-sided palate, and extraordinarily large tympanic bulla.

Habitat. Aardwolves are primarily found on open, grassy plains or in bush country, but can live in a range of habitats with rainfall between 100-800 mm. They are most common where rainfall is 100-600 mm. They do not occur in forests or pure desert and are independent of drinking water. The northern subspecies occurs in grasslands and tree savannas of the Somali-Masai Arid Zone and the southern subspecies in the Southern Savanna and South-west Arid Zone.

Food and Feeding. Aardwolves are solitary foragers and feed almost exclusively on Trinervitermes termites, usually on one species in each particular region: 1. bettionianus in East Africa, 1. rhodesiensis in Zimbabwe and Botswana and 71. trinervoides in South Africa. These termites are largely avoided by other termite-eating mammals due to the noxious terpenoid chemicals secreted by the soldier termites, to which the Aardwolfis uniquely tolerant. In addition to the lack of competition, Aardwolf preference for this termite genus is likely due to the fact that these termites regularly congregate at night in large aboveground foraging parties. The termites are licked directly from the soil surface, and are easily obtainable in large quantities. Also, unlike true harvester termites, Trinervitermes forage throughout the year, making them a dependable year-round food source. Due to the small size of Trinervitermes and the wide dispersion of colonies, female Aardwolves must forage for at least six hours a night, during which up to 300,000 termites/night (1-2 kg) are consumed. Foraging Aardwolves travel approximately 1 km /h, with their ears cocked forward and head bentslightly down, following an erratic zig-zag route. Because they often approach termite colonies from downwind, and approach with directed movement before termites could be seen,it appears that termite foraging parties are detected at least partially by smell. However, the hearing of the Aardwolf is particularly acute and is assumed to play a role in colony detection. The average time spent foraging at individual termite patches was 20-28 seconds in East Africa, but in drier Namibian grassland, Aardwolves spent an average of 1-8 and 9-2 minutes at each patch in consecutive years of observation. In South Africa, a newly weaned four-month old cub spent an average of only eleven seconds at each patch, and juveniles frequently are seen vomiting after feeding on Trinervitermes, indicating that tolerance to the chemical secretions of Trinervitermes soldiers increases with age. Even adult Aardwolves maintain some aversion to the terpene chemicals, because they will avoid feeding on mounds under repair, where typically only dense concentrations of soldiers are found at the surface. Other surface-foraging termites, particularly Hodotermes and Microhodotermes ( South Africa), Odontotermes and Macrotermes species (East Africa), make up a larger proportion of the diet when Trinervitermes are seasonally uncommon or unavailable, as during winter (May-August) in South Africa, and during the rainy season in East Africa. However, these species forage aboveground in much smaller parties (10-20 individuals vs. 4000 in Trinervitermes) and the reduced winter availability of Trinervitermes in South Africa results in a significant seasonal reduction in Aardwolf body weight and field metabolic rate. Aardwolves here were found to consume only one-sixth the number of termites in winter that they did in summer. Winter is also the highest period of mortality in Aardwolf cubs, which are 7-10 months old at this time, further indicating that this is a period ofsignificant energetic stress. Other termites found in fecal samples have included Odontotermes, Macrotermes, and Lepidotermes that are not surface-foraging species and therefore not important components of the Aardwolf diet. Occasional additional food items include ants and Coleopterans, yet the Aardwolf appears to be surprisingly inefficient at foraging on non-termite insects. Due to the high degree of specialization of its tongue for licking small arthropods, and the almost complete degeneration ofits cheek teeth, it is thought that they are unable to handle larger food items, making the species highly dependent on Trinervitermes. This dependence is supported by the absence of Aardwolves from Zambia and central and western Africa, where surface foraging Trinervitermes are either uncommon or available only a small part of the year. Aardwolves defecate in middens (also called latrines). The first defecation occurs when they exit the burrow in the evening and is typically very large, weighing up to 1 kg. Defecations are typically covered with soil. This practice of concentrating and burying their faeces, which retains some of the terpene smell of the soldier termites, has been suggested as a way of reducing the probability that an Aardwolf will mistake its own faeces for a termite colony when it is foraging. Up to 20 middens may be located in a territory.

Activity patterns. Predominantly nocturnal, in South Africa Aardwolves are generally active for 8-9 hours a day in summer but only 3-4 hours a day in winter. In summer, they generally leave the den within an hour after sunset and return 1-4 hours before sunrise. However, during winter, some diurnal activity may be observed. Aardwolves typically become active up to an hour before sunset and return to their dens after 3—4 hours of foraging. A higher proportion of their time is spent feeding in winter than in summer, and a relatively large portion of the activity of both males and females in winter (12:6%) consists of breeding activities (e.g. courtship/copulation). Inactive hours during the day are spent in underground dens, which provide refuge from temperature extremes and predators, particularly Black-backed Jackals. Dens also function importantly in cub-rearing. Nighttime rest periods are also often spent near or inside dens. A territory may include up to ten different den holes, which are typically spring hare burrows that have been enlarged by Aardwolves.

Movements, Home range and Social organization. A social unit, which occupies a welldefined territory throughout the year, consists of a male-female pair and their most recent offspring. All natal animals disperse from the territory, usually 1-2 months before birth of the nextlitter. Pair bonds arefairly stable lasting 2-5 years. Males without mates (due to death or abandonment by females) establish pair bonds with adjacent females and may abandon their originalterritories. Territory size ranges from 1-5 km? in East Africa to 3-8 km? in South Africa, and appears to be negatively related to the density of available termite mounds. Territories in the Northern Cape Province of South Africa generally supported 3000 termite mounds with an average of 55,000 termites/mound. Aardwolf density reaches 1 adult /km? in optimal habitat. Territories are maintained primarily by scent marking, which is concentrated along territory boundaries, but direct interactions between neighboring residents also occasionally occur. Both males and females actively defend territorial boundaries. Chasing and fighting, with manes raised, occurs between same-sex individuals defending territories. Intruders encountered within the territory are usually chased to the boundary and mutual avoidance is generally practiced along boundary areas. If physical contact occurs both combatants drop to their carpals and bite at each others’ necks. Although territorial behavior is exhibited by males and females,it differs between mating (June andJuly in South Africa) and non-mating seasons. Direct fights between Aardwolves appear restricted to the mating season. Whereas females tend to stay within territory boundaries year round, male behavior undergoes a marked change at the start of the mating season. After an approximately one-month “scouting” period at the beginning of the mating season, when males make frequent extra-territorial movements, yet largely refrain from pasting outside the territory, they begin more aggressive extra-territorial pasting. Their movements outside the territory continue to increase, peaking in frequency about a week before females come into estrus. These excursions are suggested to be advertizements of quality to both males and females in surrounding territories. Males engage in consecutive over-markings by pasting on particular grass stalks; the less aggressive, and apparently less fit, individual will eventually cease pasting, thus “losing” the contest. During pre-estrus females also increase their rate of pasting, primarily along territory boundaries and just outside them, apparently to encourage visits by extra-pair males. Visiting males during this period frequently “flirt” with resident females and chase or fight males that they encounter. “Flirting” typically involves the male running toward the female, then veering off and prancing past with his tail raised. However, by the time the female is in estrus (lasting 1-3 days) she is typically left with only her resident male, and potentially an aggressive neighbor. As in Striped Hyenas, there have been cases in which two male Aardwolves shared a territory with a female, both males mating with her and both guarding her cubs, but this appears to be exceptional and rare. Aardwolves are remarkably antisocial outside the breeding season. Members of resident mixed-sex pairs feed alone and typically ignore each other when they meet. Unlike the other three hyaenids, Aardwolves usually do not engage in greeting ceremonies between familiar individuals, with the exception of an occasional muzzle to muzzle sniff between mother and cub. In South Africa, nightly distance traveled by foraging females ranged from 1-5 to 9-1 km (average 4-2 km). Summer travel distances ranged from 8-12 km per night, whereas winter distances were highly variable (from less than 3 km to more than 24 km) depending on whether males were conducting extra-territorial mating forays. Travel speed is 2-3 km/h when not feeding, and about I km/h when feeding intensely. Aardwolves return to underground burrows during the day. There are typically 5-6 dens per territory. Dens are used for only 1-2 months at a time, and mates rarely use the same dens concurrently. Because Aardwolves rarely interact, the primary form of communication is olfactory. Like the other three hyaenids, the Aardwolf engages in scent marking behavior called pasting, during which a strong-smelling, yellowish-orange secretion (which quickly turns black) is deposited onto grass stalks from an extruded anal gland, located just above the anus. In addition to marking frequently at dens and latrines, which generally are not associated with territory boundaries, Aardwolves appear to use pasting as a means of territory defense. Boundary marking occurs most frequently, and is most concentrated along borders where neighboring Aardwolves maintain territories. Pasting is generally frequent, occurring about twice every 100 m of travel, and about 200 times per night, with males pasting more than females. Based on experiments with translocated scent marks, information conveyed in scent marks appears to include the sex, female reproductive state, and individual identity, at least in the case of resident neighbors, partners, and self-recognition. Outside the mating season, pasting outside territory boundaries is rare if not nonexistent, but this behavior, particularly by males, changes notably during mating periods. Even though direct interactions are rare, Aardwolves possess an impressive visual display, during which the hairs along the mane are erected, resulting in a near doubling of the apparent size of the animal. This is used in intraspecific aggressive interactions involving territory defense and in interspecific defensive interactions. Although generally a silent species, the most comprehensive analysis of the vocal repertoire of Proteles identified nine distinct sound types: “purr”, whine, jaw click, lip smack, growl, snarl, bark, squeal, and a whizzing sound which was only documented in one individual. Agonistic vocalizations are relatively diverse and increase in intensity in the following order: lip smack/jaw click, growl, snarl, bark. Squeals are heard only in cubs and appear to represent begging to mothers. The whineelicits a variety of reactions depending on the addressee and addressor, but likely functions as an appeasing or reassuring sound. As in striped and brown hyenas, Aardwolves lack a loud, longdistance vocalization like the whoop of spotted hyenas.

Breeding. Monogamous, yet during the mating season extra-pair copulations can be common (40% in South Africa). Strictly seasonal breeding in the Northern Cape where most mating occurs during the first two weeks ofJuly. Females give birth every year in early October to 1-4 cubs (average of 2-5), after a 90day gestation period. In more northern parts of the range, breeding seasons appear to be less restricted. Estrus lasts 1-3 days but females may cycle again within two weeks if fertilization does not occur. Copulation lasts from 1-4-5 hours during which multiple ejaculations occur. Copulations may be interrupted by extra-pair males and in some cases females copulate with these new males. Cubs are born in a den and rarely emerge above ground during the first month. By three months, cubs have begun making short excursions from the den, usually accompanied by an adult. Weaning occurs around four months, and by this time cubs begin foraging alone within the territory. After weaning, cubs spend little time with their parents, are independent by about seven months, and are excluded from the territory soon after, usually by one year of age. Cubs grow quickly, reaching adult body mass by 3:6 months. Thisis likely an adaptation to maximize survival of cubs through their first winter, when cub mortality is highest. Sexual maturity is reached by 1-8 years. Each resident breeding male guards the female’s cubs during the period of den dependence. This is energetically costly asit typically leaves the males only 2-3 hours of foraging time before sunrise, compared to at least six hours for females. Due to the frequency of extrapair copulations, cuckoldry appears to be an established aspect of the mating system (“overt cuckoldry”), and males are likely to frequently help raise litters of mixed paternity or sired entirely by other males. Currently this appears to be unique among mammals.

Status and Conservation. Listed as a species of Least Concern on The IUCN Red List. Due to their shy and nocturnal nature, Aardwolves are probably more common than usually believed. That notwithstanding, Aardwolves in southern Africa generally occur outside of protected areas, and the primary threat in these locationsis indirect poisoning aimed at locust outbreaks. Poisoning events can result in the death of up to half the local adult population and all the cubs. Within protected areas, the most important mortality sources are severe drought and predation on cubs by Black-backed Jackals. Human-caused mortality also occurs as a result of direct persecution from farmers suspecting Aardwolf involvement in lamb predation, harvesting of Aardwolves as a food source, and indirect persecution during organized hunting for jackals. Aardwolves may also be killed by vehicles during the night. However, all these other mortality sources appear insignificant relative to poisoning, jackal predation and drought. Across its range, habitat fragmentation and isolation may be the most serious threat to long-term population viability; however,its dependence on habitat preferred for use in livestock grazing makes extensive habitat loss improbable.

Bibliography. Anderson, M.D. & Richardson (2005), Anderson, M.D. et al. (1992), Cooper & Skinner (1979), Kingdon (1971-1982), Koehler & Richardson (1990), Koepfli et al. (2006), Kruuk & Sands (1972), Mills & Hofer (1998), Peters & Sliwa (1997), Richardson (1985, 1987a, 1987b, 1987c, 1990, 1991), Richardson & Bearder (1984), Richardson & Levitan (1994), Skinner & Van Aarde (1986), Sliwa & Richardson (1998), Smithers (1983), Sparrman (1783), Van Jaarsveld (1993), Van Jaarsveld et al. (1995), Werdelin & Solounias (1991), Williams et al. (1997).

Figures

1. Aardwolf (Proteles cristata), 2. Spotted Hyena (Crocuta crocuta), 3. Striped Hyena (Hyaena hyaena), 4. Brown Hyena (Parahyaena brunnea)

Subspecies and Distribution. P. c. cristata Sparrman, 1783 — E African coast (S Egypt , Sudan , Eritrea , Djibouti , Ethiopia , Somalia , Kenya , NE Uganda to C Tanzania ). P. c. septentrionalis Rothschild, 1902 — most of S Africa (S Angola , S Zambia , SW Mozambique , Namibia , Botswana , Zimbabwe , Swaziland , Lesotho , and South Africa ).