Spotted Hyena

Spotted Hyena
Fossil range: Late Pliocene - Recent
Ngorongoro Park, Tanzania
Conservation status

Least Concern (IUCN 3.1)[1]
Scientific classification
Kingdom: Animalia
Phylum: Chordata
Class: Mammalia
Order: Carnivora
Family: Hyaenidae
Genus: Crocuta
Species: C. crocuta
Binomial name
Crocuta crocuta
(Erxleben, 1777)[2]
Spotted Hyena range

The spotted hyena (Crocuta crocuta) also known as laughing hyena, is a carnivorous mammal of the family Hyaenidae, of which it is the largest extant member. Though the species' prehistoric range included Eurasia extending from Atlantic Europe to China,[3] it now only occurs in all of Africa south of the Sahara save for the Congo Basin.[4] Spotted hyenas live in large matriarchal communities called clans, which can consist of up to 80 individuals.[2]

Though often mislabeled as cowardly scavengers, spotted hyenas derive the majority of their nourishment by hunting medium sized ungulates,[2] and frequently clash with lions over food and territory.[5] They are highly intelligent among the carnivora, with studies indicating that their social intelligence is on par with some primate species.[6][7]

The spotted hyena features prominently in African mythology and folklore, where its portrayal varies from being a bringer of light, to a symbol of immorality and depravity.[8]

Contents

Evolution

Skull of Crocuta crocuta spelaea

It is thought that the ancestors of the spotted hyena branched off from the true hyenas (striped and brown hyenas) during the Pliocene era, 5.332 million to 1.806 million years ago. Ancestral spotted hyenas probably developed social behaviours in response to increased pressure from rivals on carcasses, thus forcing them to operate in teams. Spotted hyenas evolved sharp carnassials behind their crushing premolars, therefore they did not need to wait for their prey to die, as is the case for brown and striped hyenas, and thus became pack hunters as well as scavengers. They began forming increasingly larger territories, necessitated by the fact that their prey was often migratory, and long chases in a small territory would have caused them to encroach into another clan's turf.[9] The evolution of pack behaviour in hyenas likely influenced the ancestors of lions into first forming prides, in order to better defend their kills.[10][11] According to the fossil record, the species first evolved in the Indian Subcontinent. Spotted hyenas colonized the Middle East, Africa and the Ice Age plains of Eurasia extending from Atlantic Europe to China where a large subspecies known as C. c. spelaea or "cave hyena" developed as a response to the cold climate.[3] Naturalists and paleontologists originally assumed that the cave hyena was a separate species from the spotted hyena, due to large differences in fore and hind extremities. This was first put into question by Björn Kurtén, who stated “[...] there is evidence that this European population was continuous with southern, typical representatives of the nominate subspecies”. This was corroborated by genetic analysis' in 2004, showing no differences in DNA between the two populations.[12] With the decline of grasslands 12,500 years ago, Europe experienced a massive loss of lowland habitats favoured by cave hyenas, and a corresponding increase in mixed woodlands. Cave hyenas, under these circumstances, would have been outcompeted by wolves and humans which were as much at home in forests as in open lands, and in highlands as in lowlands. Cave hyena populations began to shrink after roughly 20,000 years ago, completely disappearing from Western Europe between 14-11,000 years ago, and earlier in some areas.[13] The spotted hyena only vanished from the Middle East in the early Holocene around 8000 years ago, and was replaced in this region by the striped hyena. Since then, it has been confined to Sub-Saharian Africa.[3]

History, systematics and naming

Crocotta, as illustrated in a medieval bestiary

It is thought that the spotted hyena conforms to the chaus described by Pliny the Elder, which was later described by Linnaeus as being part of the cat tribe. It is also thought to be the Crocotta of Strabo, which he thought to be a wolf-dog hybrid.[14] Sculptured representations indicate that the species was rarely encountered by the Ancient Egyptians, who considered them exotic enough to include them in their menageries of foreign animals and to exclude them from their sacred animals.[14] Certain scholars interpret Aristotle's inaccurate description of striped hyenas as being hermaphroditic animals as being a confusion between the striped and spotted species.[15]

Systematics

In his 12th-edition of Systema Naturæ, Linnaeus placed hyenas into the genus Canis, between wolves and foxes. Brisson had already given the form a generic distinction under the name Hyæna. In his own edition of Linnaeus' Systema Naturæ, Johann Friedrich Gmelin gave the spotted species the binomial name Canis crocuta, though Thomas Pennant had previously described it under the title of Hyæna, and placed it under the category of "Spotted Hyænas". Georges Cuvier made Hyænas into the last subdivision of digitigrades, following viverrids and preceding felids.[15] Cuvier was convinced that there were at least two different species of spotted hyena, based on regional differences in coat colours. However, subsequent naturalists did not accept this, for although they noted coat variations, there were no other differences to fully warrant classing them as different species.[16] John Edward Gray later brought the spotted hyena under the Felidae, placing it within a category including other hyenas and the aardwolf. M. Lesson arranged the hyænids under his third section of digitigrades, a section consisting of animals lacking a small tooth behind the lower molar. The spotted hyena was placed between aardwolves and cats, and was termed Hyæna capensis.[15]

Local and indigenous names

Several languages of Africa lack species specific names for hyenas: for example, the spotted and striped species have identical names in Dioula, Fulbe, Swahili, Malinké, Mòoré, Ngambaye, Oulof and Peuhl. In other languages, other species may simply be termed "small spotted hyena", such as in Swahili, where the spotted hyena is termed fisi and the Aardwolf fisi ndogo.[17]

Afrendille: Walaba[18] Afrikaans: Gevlekte hiëna[19] Amharinja: Djibb[19] Arabic (CAR) and Arabic (Chad): Marfaïn[19] Arabic (North Africa):D'ba[19] Arabi (Ethiopia): Dibb Ateso: Ibuin[18] Avukaia: Labagu[19] Babouté: Mangou[19] Baguirmien: Niougo[19] Baka: Libagu[19] Bakola: Mazzobé[19] Bambara: Namakoro, souroukou[19] Banda: Bongo[19] Bechuana: Piri, phiri[19] Bemba (Zambia): Chimbwi[19] Bornouan: Boultou[19] Creole: Lobo[19] Danakil: Jangóula[19] Dioula: Suruku, namakoro[19] Elkoni: Makatiet nyenegea[18] English: Spotted hyena, Tiger wolf, Wolf of the Cape colonists[16] French: Hyène tachetée[19] Fula, Futa and Fulbe: Bonoro, fourou[19] Galaorabéjsa: Wårabéssa, orabéjsa[19] Gambe: Mangili[19] German: Tüpfelhyäne, Fleckenhyäne[19] Gouragi: Woraba[19] Gourmatche: Namlino[19] Harari: Worábba[19] Hassānīya Arabic: Guervave[19] Haussa: Koura[19] Herero: Mbúngu-mbidíwa[19] Ila (Zambia): Kabwenga[19] Jita: Imembe[19] Kalenjin: Kimatet[18] Kaonde: Mungolwe[19] Karamojong: Ebu, Etutui[18] Kichagga: Ingurunju, ifulu[19] Kigogo and kikongo: Misi[18][19] Kikamba and Kisukuma: Mbiti[19] Kikondo: Mbulu[19] Kiliangulu: Warabes[18] Kiluba: Kimburi[19] Kimeru: Mbitingaau[19] Kinyarwanda: Impysi[19] Kinyaturo: Mpiti[18] Kinyiha: Ipatama[19] Kipare and Kizigua: Ibau[18] Kirangi: Mbichi[19] Kisungwa: Fifi[19] Koniagui: Iriguni[19] Kota: Massoba[19] Kotoko: Machi[19] Kunda: Tika[19] Jita: Imembe[18] Kikuyu: Hiti[18] Kimeru: Mbitingaau[18] Kinyiha: Impatama[18] Kirangi: Mbichi[18] Kisukuma, Kikamba and Kimaragoli: Mbiti[18] Kisungwa: Fifi[18] Swahili: Fisi, Nyangao[18] Kitaita: Mbisi[18] Luganda and Runyoro: Empisi[18] Lugbara: Rara[18] Luhya: Namunyu[18] Luo: Otoyo[18] Lwo: Lagwara[18] Madi: Ebowu[18] Masai: Ondilili, Oln'gojine[18] Sebei: Mangatiet[18]

Physical description

Skeleton
Skull, as illustrated by Frédéric Cuvier. Note the disproportionately large carnassials and premolars adapted for bone consumption[9]
Head and chest

Spotted hyenas are the largest of extant hyenas. Their fur is shorter than those of striped hyenas, and their manes less full.[20] Spotted hyenas have powerful forequarters and necks which rival those of leopards,[21] though comparatively small hindquarters. The rump is rounded rather than angular, which prevents attackers chasing from behind getting a firm grip on it.[22] Female spotted hyenas are considerably larger than males, weighing 12% more.[9] Adults measure 95.0—165.8 cm in body length, and have a shoulder height of 70.0-91.5 cm.[18] Adult male spotted hyenas in the Serengeti weigh 40.5—55.0 kg (89—121 lb), while females weigh 44.5—63.9 kg (98—141 lb). Spotted hyenas in Zambia tend to be heavier, with males weighing on average 67.6 kg (149 lb), and females 69.2 kg (153 lb).[22] Macdonald (1992) gives a maximum weight of 81.7 kg (180 lb),[9] while Kingdon (1977) gives one of 86 kg (190 lb).[18] The skulls of Zambian hyenas are also 7% longer and wider than those of Serengeti populations.[22] It has been estimated that adult members of the now extinct Eurasian populations weighed 102 kg (225 lbs).[23]

Their dentition is more dual purposed than that of other modern hyena species, which are mostly scavengers: the upper and lower third premolars are conical bone-crushers, with a third bone-holding cone jutting from the lower fourth premolar. Spotted hyenas also have carnassials behind their bone-crushing premolars, the position of which allowing hyenas to crush bone with their premolars without blunting their carnassials.[9] The carnassials themselves are proportionately larger than those of other carnivorous mammals.[24] Although they possess disproportionately large teeth to counteract wear, three year old spotted hyenas have teeth as worn as those of six year old lions.[9] Combined with large jaw muscles and a special vaulting to protect the skull against large forces, these characteristics give spotted hyenas a powerful bite which can exert a pressure of 800 kgf/cm2 (11,400 lbf/in²),[9] which is 40% more force than a leopard can generate.[25] An experiment conducted by Savage (1955) demonstrated how the jaws of spotted hyenas outmatch those of brown bears in bonecrushing ability,[26] and free ranging hyenas have been observed to crack open the long bones of giraffes measuring 7 cm in diameter.[27] Although once thought to have the most powerful jaws among extant carnivorous mammals, other animals such as the Tasmanian Devil have been proven to have even stronger bites.[28]

With the exception of size, there is little sexual dimorphism in spotted hyenas. The external genitalia of females closely resemble those of males: the 15 cm (6 inch)[9] clitoris is similar in shape and position as a penis, and is capable of erection.[22] The only visible difference between the penis of male spotted hyenas and the clitoris of females is that the latter's organ has a blunter tip.[9] The labia are fused together into a pair of fibrous sacs resembling a scrotum. Typically, when observing sexually mature animals, naturalists use the presence of nipples as an indicator of gender when observing spotted hyenas at a distance.[22] Females have two nipples and rarely four.[29] The colour and spotting of the coat varies with age and individual. The number of spots tends to decrease with age.[22]

Although there are no different extant subspecies, spotted hyenas do display a degree of regional variation, particularly in their southern range, where they tend to be darker and browner in colour, particularly on the back and legs. Due to this darker hue, the spots of southern spotted hyenas are less defined and angular than their cousins on the West Coast. Also, the fur is longer in the South African form, particularly around the ears.[16] Specimens from the former cameroons, the Epukiro district of former German West Africa and northern and western Togo have proportionately longer tails than average. The spots of Cameroon spotted hyenas are greatly elongated in the hind region, with the main spots being almost streaks.[30]

Spotted hyenas have a powerful night vision, which allows them to recognise each other in complete darkness, even if they are downwind.[31]

Behavior

Spotted hyenas will rest and give birth in dens, which they rarely dig themselves: they will often use the abandoned lairs of warthogs, springhares and jackals. A single den can house several females and dozens of cubs at once.[29] Unlike grey wolves, it is not uncommon for spotted hyenas to accommodate cubs of different litters in one den.[32] Spotted hyenas will sometimes live in close proximity to warthogs, sharing mudholes and sleeping within a few metres of each other.[33] Spotted hyenas may sleep in the open if the weather is not too hot, but otherwise they will rest near lakes, streams or in mud or dense shrubs.[34] Unlike most social carnivores, spotted hyenas still display some atavistic behaviours of their solitary ancestors: spotted hyenas still head out for food alone, but later return to their community.[35] Like other hyenas, spotted hyenas have two anal scent glands, which open into the rectum just inside the anal opening,[36] though these glands are less elaborate than those of other hyena species.[9] The white paste produced by these glands is deposited on grass stalks, and produce a powerful soapy odour which even humans can detect. Pasting is performed on a number of different occasions, such as when walking alone, when around a kill, when lions are present, by males and cubs near dens, and most frequently by parties of hyenas at territorial boundraries. Pasting is often followed by scratching the ground with their forepaws, which adds further scents from their interdigital glands.[36]

Social behavior

Spotted hyenas are more social than grey wolves, but their groups are not as closely knit as African wild dogs.[32] Spotted hyena societies are more complex than those of other carnivorous mammals, and have been reported to be remarkably similar to those of cercopithecine primates in respect to group size, structure, competition and cooperation. Like primates, spotted hyenas use multiple sensory modalities, recognise individual conspecifics, are conscious that some clan-mates may be more reliable than others, recognise 3rd party kin and rank relationships among clan-mates, and adaptively use this knowledge during social decision making. Also, like cercopithecine primates, dominance ranks in hyena societies are not correlated with size or aggression, but with ally networks.[6] Group size is variable; a "clan" of spotted hyenas can include 5–90 members and is led by a single alpha female called the matriarch. Scientists theorise that female hyena dominance could be an adaptation to the length of time it takes for cubs to develop the massive skulls and jaws, and intense feeding competition within clans, thus necessitating greater attention and dominating behaviours from females.[37] Female hyena dominance is sometimes explained by the unusually high concentration of androgens produced by the ovaries. However adult hyena males display a higher concentration of androgens than adult hyena females. This would suggest that adult concentrations of androgens probably do not account for the difference of social dominance.[38]

Reproduction and development

Spotted Hyena and two cubs, Ngorongoro Crater, Tanzania
Young Spotted Hyenas rest on a road in the Kruger National Park in South Africa. Note the well defined spots, which will fade with age
Skull of a newborn spotted hyena from the Muséum national d'histoire naturelle

Spotted hyenas are not seasonal breeders, and can reproduce at any time of the year, though a birth peak does occur during the wet season. Females are polyestrous, with an estrous period lasting two weeks.[39] The average litter consists of two cubs, with three occasionally being reported.[39] Mating in spotted hyenas is a relatively short affair which typically only occurs at night with no other hyenas present. Males will show submissive behaviour when approaching females in heat, even if the male outweighs its partner. There is no copulatory tie, as in canids.[29] Females usually favour younger males born into, or joined into the clan after they were born. Older females show a similar preference, with the addition of preferring males with whom they have had long and friendly prior relationships.[40] Passive males tend to have greater success in courting females than aggressive ones.[41] Males take no part in the raising of young.[32] The length of the gestation period tends to vary greatly, though 110 days is the average length of time.[39] In the final stages of pregnancy, dominant females provide their developing offspring with higher androgen levels than lower-ranking mothers do. The higher androgen levels - the result of high concentrations of ovarian androstenedione - are thought to be responsible for the extreme masculinization of female behavior and morphology.[42] This has the effect of rendering the cubs of dominant females more aggressive and sexually active than those of lower ranking hyenas: high ranking male cubs will attempt to mount females earlier than lower ranking males.[43]

Birth is difficult, as females have to give birth through their narrow clitoris. Also, spotted hyena cubs are the largest carnivoran cubs relative to their mother's weight.[9] In captivity, many cubs of first time mothers are stillborn because of the long labour times involved, and in the wild, it is estimated that 10% of first time mothers die during labour.[44] The cubs are born with soft, brownish black hair, and weigh on average 1.5 kg.[29] Unique among carnivorous mammals, spotted hyenas are also born with their eyes open and with 6–7 mm long canine teeth and 4 mm long incisors. Also, cubs will attack each other from the moment they are born. This is particularly apparent in same sexed litters, and can result in the death of the weaker cub.[9] This neonatal siblicide can amount to 25% of overall spotted hyena cub mortality factors.[45] Spotted hyena hierarchy is nepotistic: the offspring of dominant females automatically outrank adult females subordinate to their mother,[9] though they can lose their privileges if the mother dies.[45] Females are very protective of their cubs, and will not tolerate other adults, particularly males, approaching them. Spotted hyenas exhibit adult behaviours very early in life: cubs have been observed to ritually sniff each other and mark their living space before the age of one month. Within ten days of birth, they are able to move at considerable speed. Cubs begin to lose the black coat and develop the spotted, lighter coloured pelage of the adults at two-three months. They begin to exhibit hunting behaviours at the age of eight months, and will begin fully participating in group hunts after their first year.[29]

Lactating females can carry 3–4 kg (6.5-9 lb) of milk in their udders.[9] Spotted hyena milk is very rich, having the highest protein content (14.9%) of any terrestrial carnivore. The fat content (14.1%) is second only to the polar bear, so unlike lions and wild dogs, they can leave their cubs for about a week without feeding them.[46] Cubs will nurse from their mother for 12 or 16 months, though they can process solid food as early as three months.[29]

Spotted hyenas reach sexual maturity at the age of three years.[39] The average lifespan in zoos is 12 years, with a maximum of 25 years.[39]

Dietary habits

An adult and subadult spotted hyena feed from a giraffe carcass amongst a large number of vultures

Spotted hyenas are better equipped for scavenging than other African predators: not only are they able to splinter and eat the largest ungulate bones, they are also able to digest them completely. Spotted hyenas can digest all organic components in bones, not just the marrow. Any inorganic material is excreted with the faeces, which consist almost entirely of a white powder with few hairs. They react to alighting vultures more readily than other African carnivores, and are more likely to stay in the vicinity of lion kills or human settlements.[24] Wildebeest are the most commonly taken medium sized ungulate prey item in both Ngorongoro and the Serengeti, with zebra and Thomson's gazelles coming close behind.[47] Cape buffalo are rarely attacked due to differences in habitat preference, though adult bulls have been recorded to be taken on occasion.[33] Spotted hyenas have also been found to catch fish,[48] tortoises,[49] humans,[50] black rhino,[51] hippo calves,[52] young African elephants,[53] pangolins,[49] pythons, and a large number of different ungulate species.[47] The fossil record indicates that Eurasian Spotted hyenas in what is now the Czech Republic primarily fed on Przewalski's Horses. Other prey included woolly rhinoceros, Reindeer, Steppe Wisent, Irish elk, chamois and ibex.[54] In Italy, their prey consisted of red deer, aurochs, horses, roe deer, fallow deer, wild boar and ibex.[13] Spotted hyenas are thought to be responsible for the dis-articulation and destruction of some cave bear skeletons. Such large carcasses were an optimal food resource for the hyenas, especially at the end of winter, when food was scarce.[54] However, they were less successful than cave lions in navigating through cave bear dens, due to their inferior climbing abilities.[55]

A single spotted hyena can eat at least 14.5 kg of meat per meal.[56] Although spotted hyenas act aggressively toward each other when feeding, they compete with each other mostly through speed of eating, rather than by fighting as lions do.[57] When feeding on an intact carcass, spotted hyenas will first consume the meat around the loins and anal region, then open the abdominal cavity and pull out the soft organs. Once the stomach, its wall and contents are consumed, the hyenas will eat the lungs and abdominal and leg muscles. Once the muscles have been eaten, the carcass is disassembled and the hyenas carry off pieces to eat in peace.[56] Spotted hyenas are adept at eating their prey in water: they have been observed to dive under floating carcasses to take bites, then resurface to swallow. A single hyena can take less than two minutes in eating a gazelle fawn,[47] while a group of 35 hyenas can completely consume an adult zebra in 36 minutes. Spotted hyenas do not require much water, and typically only spend 30 seconds drinking.[56]

Hunting behavior

Unlike other large African carnivores, spotted hyenas do not preferentially prey on any species, and only buffalo, giraffe and plains zebra are significantly avoided. Spotted hyenas prefer prey with a body mass range of 56–182 kg, with a mode of 102 kg.[58] When hunting medium to large sized prey, spotted hyenas tend to select certain categories of animal: young animals are frequently targeted, as are old ones, though the latter category is not so significant when hunting zebras, due to their aggressive antipredator behaviours.[59] Unlike grey wolves, spotted hyenas rely more on sight than smell when hunting, and do not follow their prey's prints or travel in single file.[32]

Spotted hyenas usually hunt wildebeest either singly, or in groups of two or three. They catch adult wildebeest usually after 5 km chases at speeds of up to 60 km/h. Chases are usually initiated by one hyena, and with the exception of cows with calves, there is little active defense by the wildebeest herd. Wildebeest will sometimes attempt to escape hyenas by taking to water, though in such cases, the hyenas almost invariably catch them.[33] Zebras require different hunting methods to those used for wildebeest, due to their habit of running in tight groups and aggressive defence from stallions. Hyenas seem to plan on hunting zebras in advance, as they tend to indulge in activities such as scent marking before setting off, a behaviour which does not occur when they target other prey species. Typical zebra hunting groups consist of 10-25 hyenas. During a chase, zebras typically move in tight bunches, with the hyenas pursuing behind in a crescent formation. Chases are usually relatively slow, with an average speed of 15–30 km/h. A stallion will attempt to place itself between the hyenas and the herd, though once a zebra falls behind the protective formation it is immediately set upon, usually after a chase of 3 km. Though hyenas may harass the stallion, they usually only concentrate on the herd and attempt to dodge the stallion's assaults. Unlike stallions, mares typically only react aggressively to hyenas when their foals are threatened. Unlike wildebeest, zebras rarely take to water when escaping hyenas.[59] Once prey is caught, spotted hyenas will kill their prey by eating it alive.[33]

Spotted hyenas will increase their kill rate during the calving seasons of their prey,[60] or when they are frequently displaced from their kills by other predators.[57]

Interspecific predatory relationships

In areas where spotted hyenas and lions are sympatric, the two species occupy the same ecological niche, and are thus in direct competition with one another. In some cases, the extent of dietary overlap can be as high as 68.8%.[58] Lions typically ignore spotted hyenas, unless they are on a kill or are being harassed by them. Spotted hyenas themselves tend to visibly react to the presence of lions, whether there is food or not. Lions will readily appropriate the kills of spotted hyenas: in the Ngorongoro crater, it is common for lions to subsist largely on kills stolen from hyenas, causing the hyenas to increase their kill rate. Lions are quick to follow the calls of hyenas feeding, a fact which was proven by Dr. Hans Kruuk, who found that lions repeatedly approached him whenever he played the tape-recorded calls of hyenas feeding.[57] When confronted on a kill by lions, spotted hyenas will either leave or wait patiently at a distance of 30–100 metres until the lions have finished.[61] In some cases, spotted hyenas are bold enough to feed alongside lions, and may occasionally force the lions off a kill.[29] Spotted hyenas usually prevail against groups of lionesses unaccompanied by males if they outnumber them 4:1.[62] The two species may act aggressively toward one another even when there is no food involved. Lions may charge at hyenas and maul them for no apparent reason: one male lion was filmed killing two matriarch hyenas on separate occasions without eating them,[45] and lion predation can account for up to 71% of hyena deaths in Etosha. Spotted hyenas have adapted to this pressure by frequently mobbing lions which enter their territories.[63] Occasionally, lion prides and spotted hyena clans may engage in full warfare, as with a case in early April, 1999 in Ethiopia, in which 6 lions and 35 hyenas were killed over a two week period.[5] Experiments on captive spotted hyenas revealed that specimens with no prior experience with lions act indifferently to the sight of them, but will react fearfully to the scent.[29]

Although cheetahs and leopards prey on smaller animals than those hunted by spotted hyenas, hyenas will steal their kills when the opportunity presents itself. Cheetahs are usually easily intimidated by hyenas, and put up little resistance,[57] while leopards, particularly males, may stand up to hyenas. There are records of some male leopards preying on hyenas.[21]

Spotted hyenas will follow packs of African wild dogs in order to appropriate their kills. They will typically inspect areas where wild dogs have rested and eat any faeces they find. When approaching wild dogs at a kill, solitary hyenas will approach cautiously and attempt to take off with a piece of meat unnoticed, though they may be mobbed by the dogs in the attempt. When operating in groups, spotted hyenas are more successful in pirating dog kills, though the dog's greater tendency to assist each other puts them at an advantage against spotted hyenas, who rarely work in unison. Cases of dogs scavenging from spotted hyenas are rare. Although wild dog packs can easily repel solitary hyenas, on the whole, the relationship between the two species is a one sided benefit for the hyenas.[57]

Spotted hyenas dominate other hyena species wherever their ranges overlap. Brown hyenas encounter spotted hyenas in the Kalahari, where the brown species outnumbers the spotted. The two species typically encounter each other on carcasses, which the larger spotted species usually appropriate. Sometimes, brown hyenas will stand their ground and raise their manes while emitting growls. This usually has the effect of seemingly confusing spotted hyenas, which will act bewildered, though they will occasionally attack and maul their smaller cousins. Similar interactions have been recorded between spotted and striped hyenas in the Serengeti.[64]

Jackals will feed alongside hyenas, though they will be chased if they approach too closely. Spotted hyenas will sometimes follow jackals during the gazelle fawning season, as jackals are effective at tracking and catching young animals. Hyenas do not take to eating jackal flesh readily: four hyenas were reported to take half an hour in eating a golden jackal. Overall, the two animals typically ignore each other when there is no food or young at stake.[57]

Spotted hyenas usually keep a safe distance from Nile crocodiles. Though they readily take to water to catch and store prey, hyenas will avoid crocodile infested waters.[57]

Now extinct spotted hyena populations living in Italy shared their range with wolves, but managed to avoid competition by inhabiting lowlands, rather than the slopes favoured by wolves. Also, spotted hyenas primarily fed on horses, while wolves targeted ibex and roe deer. However, wolves and spotted hyenas seem to display negative abundance relations over time, with wolf populations expanding in the regions where hyenas disappeared.[13]

Intelligence

Compared to other hyenas, spotted hyenas show a greater relative amount of frontal cortex exclusive to motor control functions. Studies strongly suggest convergent evolution in spotted hyena and primate intelligence.[6] A study done by evolutionary anthropologists demonstrated that spotted hyenas outperform chimpanzees on cooperative problem-solving tests: captive pairs of spotted hyenas were challenged to tug two ropes in unison to earn a food reward, successfully cooperating and learning the maneuvers quickly without prior training. Experienced hyenas even helped inexperienced clan-mates to solve the problem. In contrast, chimps and other primates often require extensive training, and cooperation between individuals is not always as easy for them.[7]

Communication

Body language

A spotted hyena in an approaching attitude, but with a high avoidance tendency[36]

Spotted hyenas have a complex set of postures in communication. When afraid, the ears are folded flat, and are often combined with baring of the teeth and a flattening of the mane. When attacked by other hyenas or by wild dogs, the hyena lowers its hindquarters. Before and during an assertive attack, the head is held high with the ears cocked, mouth closed, mane erect and the hindquarters high.[36] The tail usually hangs down when neutral, though it will change position according to the situation. When a high tendency to flee an attacker is apparent, the tail is curled below the belly. During an attack, or when excited, the tail is carried forward on the back. An erect tail does not always accompany a hostile encounter, as it has also been observed to occur when a harmless social interaction occurs. Although they do not wag their tails, spotted hyenas will flick their tails when approaching dominant animals or when there is a slight tendency to flee.[36] When approaching a dominant animal, subordinate spotted hyenas will walk on the knees of their forelegs in submission.[36]

Vocalisations

Spotted hyenas are very vocal animals, and produce a number of different calls. Generally, high pitched calls signify fear or submission, while low pitched calls accompany a high tendency to attack.[36]

The loud "whoop" is a characteristic sound of the African night[36] and is audible for over 5 km (3 miles) or more.[9] It is a rallying cry, which varies in speed and pitch according to the urgency of the situation.[36] Spotted hyenas also whoop to show off as individuals, the rate and style being an indicator of social status. Because of this, spotted hyenas whoop singly rather than in chorus as wolf packs do to display their collective strength. Although males tend to whoop more than females of similar rank, dominant females will engage in the longest bouts of whooping.[9] Giggles and grunt-laughter tend to be emitted in situations of great excitement, and perhaps indicate a conflicting tendency to flee or stay. The giggles, yells and grunts which accompany mass feeding tend to be directed at competing individuals at a carcass, and has the secondary, disadvantageous effect of attracting lions and other spotted hyenas.[29] The pitch of the laugh indicates the hyena's age, while variations in the frequency of notes used when hyenas make noises convey information about the animal's social rank.[65] Soft grunts are made by females calling their cubs.[29] When attacked, spotted hyenas will emit loud growls and whimpers.[36]

Current range and distribution

The largest known spotted hyena populations occur in the Serengeti ecosystem in Tanzania (where they number 7,200-7,700), Kruger National Park in South Africa (1,300-3,900) and the Masai Mara Game Reserve in Kenya (ca 500-1,000). Several hundred, unsurveyed individuals occur in Zimbabwean conservation areas, the Selous Game Reserve in Tanzania and the Okavango in Botswana. Spotted hyenas are considered by the IUCN to be of lower risk of extinction in Botswana, Ethiopia, Guinea Bissau, Kenya, Namibia, South Africa, Tanzania and Zimbabwe. They are a threatened species in Benin, Burundi (where they are thought to be on the verge of extinction), Cameroon, Mali, Mauritania, Niger, Nigeria, Rwanda and Sierra Leone. They are extinct in Algeria and Lesotho. There is a deficiency of data on the number of spotted hyenas in Angola, Burkina Faso, the Central African Republic, Chad, the Republic of the Congo, Côte d'Ivoire, the Democratic Republic of Congo, Djibouti, Eritrea, Equatorial Guinea, Ghana, Guinea, Malawi, Mozambique, Senegal, Somalia, Sudan, Swaziland, Togo, Uganda and Zambia.[66]

Relationships with humans

A broadside announcing the main feeding in the menagerie of Hermann von Aken in Hanover on 23 November 1830, depicting a man holding open the jaws of a spotted hyena

Prehistoric interactions

20,000 year old spotted hyena painting found in a French cave by Jacques Toubon in 1994.

Kills partially processed by Neanderthal and then by cave hyenas indicate that hyenas would occasionally steal Neanderthal kills, and cave hyenas and Neanderthal both competed for cave sites. Many caves show alternating occupations of hyenas and Neanderthals.[67] The discovery of a cave in Siberia's Altai Mountains, which showed evidence of being inhabited by spotted hyenas for about 40,000 years, lead to the speculation that the presence of spotted hyenas there could have prevented humans from crossing the Bering land bridge to the Americas, thus explaining why humans colonised the New World much later than when land bridge had formed. This scenario was brought up due to there being large numbers of fossil human remains dating back 50,000-60,000 years ago below the latitude of Mongolia, and comparatively few remains, dated back less than 12,000 years ago, further north, where hyenas ranged. The discovery of a 14,000 year old dog skull further lead to the theory that the domestication of the dog may have been a factor in aiding the eventual crossing, as dogs would have been valuable sentinels against hyena incursions into human encampments.[68]

Impacts on human culture and thought

Spotted hyenas vary in their folkloric and mythological depictions, depending on the ethnic group from which the tales originate. It is often difficult to know whether or not spotted hyenas are the specific hyena species featured in such stories, particularly in West Africa, as both spotted and striped hyenas are often given the same names.[8] In western African tales, spotted hyenas are sometimes depicted as bad Muslims who challenge the local animism that exists among the Beng in Côte d’Ivoire. In East Africa, Tabwa mythology portrays the spotted hyena as a solar animal that first brought the sun to warm the cold earth, while West African folklore generally shows the hyena as symbolizing immorality, dirty habits, the reversal of normal activities, and other negative traits. In Tanzania, there is a belief that witches use spotted hyenas as mounts.[8] In the Mtwara Region of Tanzania, it is believed that a child born at night while a hyena is crying will likely grow up to be a thief. In the same area, hyena faeces are believed to enable a child to walk at an early age, thus it is not uncommon in that area to see children with hyena dung wrapped in their clothes.[17] The Kaguru of Tanzania and the Kujamaat of Southern Senegal view hyenas as inedible and greedy hermaphrodites. A mythical African tribe called the Bouda is reputed to house members able to transform into hyenas.[69] A similar myth occurs in Mansoa. These "werehyenas" are executed when discovered, but do not revert back to their human form when killed.[17]

Spotted hyenas feature prominently in the rituals of certain African tribes. In the Gelede cult of the Yoruba people of Benin and Southwest Nigeria, a spotted hyena mask is used at dawn to signal the end of the èfè ceremony. As the spotted hyena usually finishes the meals of other carnivores, the animal is associated with the conclusion of all things. Among the Korè cult of the Bambara people in Mali, the belief that spotted hyenas are hermaphrodites appears as an ideal in-between in the ritual domain. The role of the spotted hyena mask in their rituals is often to turn the neophyte into a complete moral being by integrating his male principles with femininity. The Beng people believe that upon finding a freshly killed hyena with its anus inverted, one must plug it back in, for fear of being struck down with perpetual laughter. They also view spotted hyena faeces as contaminating, and will evacuate a village if a hyena relieves itself within village boundaries. Kujamaat hunters traditionally treat the spotted hyenas they kill with the respect due to human elders, in order to avoid retribution from malevolent hyena spirits acting on behalf of the dead animal.[8] In Maasai tradition, and that of other tribes, corpses are left in the open for spotted hyenas to eat. A corpse rejected by hyenas is seen as having something wrong with it, and liable to cause social disgrace, therefore it is not uncommon for bodies to be covered in fat and blood from a slaughtered ox.[17]

The vocalisation of the spotted hyena resembling hysterical human laughter has been alluded to in numerous works of literature: "to laugh like a hyæna" was a common proverb, and is featured in The Cobbler's Prophecy (1594), Webster's Duchess of Malfy (1623) and Shakespeares As You Like It, Act IV. Sc.1.

Attacks on humans

Illustration from Fraser's magazine showing an artist's impression of a "stag-hound" biting a spotted hyena attacking its master

Spotted hyenas are usually timid around humans, and will typically flee over a distance of 300 metres when an approaching human is detected.[57] Although spotted hyenas do prey on humans in modern times, such incidences are rare. However, according to the SGDRN (Sociedade para a Gestão e Desenvolvimento da Reserva do Niassa Moçambique), attacks on humans by spotted hyenas are likely to be underreported.[70] Hyenas are known to have preyed on humans in prehistory: human hair has been found in fossilised hyena dung dating back 195,000 to 257,000 years.[71] According to Dr. Hans Kruuk, man-eating spotted hyenas tend to be very large specimens: a pair of man-eating hyenas, responsible for killing 27 people in Mlanje, Malawi in 1962 and were weighed at 72 kg (159 lb) and 77 kg (170 lb) after being shot.[72] In 1903, Hector Duff wrote of how spotted hyenas in the Mzimba district of Angoniland would wait at dawn outside people's huts and attack them when they opened their doors.[73] According to R.G. Burton's A Book of Man-Eaters, spotted hyenas will enter human encampments without paying any notice of camp fires.[74] Victims of spotted hyenas tend to be women, children and sick or infirm men: Theodore Roosevelt wrote on how in 1908-09 in Uganda, spotted hyenas regularly killed sufferers of African sleeping sickness as they slept outside in camps.[75] When attacking sleeping people, spotted hyenas usually bite the face, and attempt to drag their victims far from other humans.[76] The Kikuyu of Kenya fear spotted hyenas more than the striped species.[77] Spotted hyenas are widely feared in Malawi, where they have been known to occasionally attack people at night, particularly during the hot season when people sleep outside. Hyena attacks were widely reported in Malawi's Phalombe plain, to the north of Michesi Mountain. Five deaths were recorded in 1956, five in 1957 and six in 1958. This pattern continued until 1961 when eight people were killed. Attacks occurred most commonly in September, when people slept outdoors, and bush fires made the hunting of wild game difficult for the hyenas.[70][73] An anecdotal news report from the World Wide Fund for Nature 2004 indicates that 35 people were killed by spotted hyenas in a 12 month period in Mozambique along a 20 km stretch of road near the Tanzanian border.[70] Attitudes toward spotted hyena attacks tend to be muted when compared to the reactions evoked in areas where striped hyenas have attacked people.[17]

Livestock predation

The degree with which spotted hyenas impact livestock varies from region to region: in the Laikipia district in Kenya, spotted hyenas have little impact on livestock compared to that perpetrated by lions, leopards and cheetahs.[78] However, total reported losses in Tanzania during 2003 amounted to US $12,846 of which spotted hyena kills were reported to account for 98.2%. In a survey taken in seven different villages outside the Serengeti National Park in Tanzania in 2007, spotted hyenas accounted for 97.7% of livestock losses to predators.[79] In the Maasai steppe landscape in Northern Tanzania, spotted hyenas frequently kill small stock (goat, sheep and calves) and dogs, and usually commit their depredations at night, thus making them harder to retaliate against than lions, which mostly attack livestock in the daytime.[80]

Spotted hyenas as pets

Spotted Hyena at the Buffalo Zoo

Spotted hyenas were occasionally present in the menageries of the Pharaohs.[14] Sir John Barrow, in his An Account of Travels Into the Interior of Southern Africa, described how spotted hyenas in Sneeuberge were trained to hunt game, writing that they were "as faithful and diligent as any of the common domestic dogs".[81] In Tanzania, spotted hyena cubs may be taken from a communal den by witchdoctors, in order to increase their status.[17] An April 2004 BBC article described how a shepherd living in the small town of Qabri Bayah about 50 kilometres from Jigjiga town in eastern Ethiopia managed to use a male spotted hyena as a livestock guardian dog, suppressing its urge to leave and find a mate by feeding it special herbs.[82] If not raised with adult members of their kind, captive spotted hyenas will exhibit scent marking behaviours much later in life than wild specimens.[29] Spotted hyenas can be very destructive: a captive, otherwise perfectly tame, specimen in the Tower of London managed to tear an 8-foot (2.4 m) long plank nailed to its recently repaired enclosure floor with no apparent effort.[83] From a husbandry point of view, hyenas are easily kept, as they have few disease problems and it is not uncommon for captive hyenas to reach 15–20 years of age.[84]

References

  1. ↑ Honer, O., Holekamp, K.E. & Mills, G. (2008). Crocuta crocuta. In: IUCN 2008. IUCN Red List of Threatened Species. Downloaded on 22 March 2009. Database entry includes a brief justification of why this species is of least concern.
  2. ↑ 2.0 2.1 2.2 Background from Hans Kruuk’s The Spotted Hyena: A Study of Predation and Social Behaviour The University of Chicago Press, Chicago 60637, 1972
  3. ↑ 3.0 3.1 3.2 Kurtén, Björn. Pleistocene Mammals from Europe
  4. ↑ Geography and Habitat from Hans Kruuk’s The Spotted Hyena: A Study of Predation and Social Behaviour The University of Chicago Press, Chicago 60637, 1972
  5. ↑ 5.0 5.1 Relationships with other predators from The Art of being a Lion by Christine and Michel Denis-Huot, White Star publishers, 2002
  6. ↑ 6.0 6.1 6.2 Journal of mammology, Vol. 88, No.3, June 2007
  7. ↑ 7.0 7.1 Hyenas Surprisingly Good at Cooperative Tasks By LiveScience Staff, posted: 28 September 2009 12:56 pm ET
  8. ↑ 8.0 8.1 8.2 8.3 "The Magicality of the Hyena: Beliefs and Practices in West and South Asia" (PDF). Asian Folklore Studies, Volume 57, 1998: 331–344. June 2008. http://www.nanzan-u.ac.jp/SHUBUNKEN/publications/afs/pdf/a1246.pdf. Retrieved 23. 
  9. ↑ 9.00 9.01 9.02 9.03 9.04 9.05 9.06 9.07 9.08 9.09 9.10 9.11 9.12 9.13 9.14 9.15 Chapter 4: Rich Man's Table from David MacDonald’s The Velvet Claw BBC books, 1992.
  10. ↑ Chapter 2: Sharpening the Tooth from David MacDonald’s The Velvet Claw BBC books, 1992
  11. ↑ Big Cat Diary: Lion by Jonathan Scott and Angie Scott, Collins; illustrated edition ISBN 0007146663
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  13. ↑ 13.0 13.1 13.2 "Comparative ecology and taphonomy of spotted hyenas, humans, and wolves in Pleistocene Italy". C. Stiner, Mary. Revue de Paléobiologie, Genève. http://www.u.arizona.edu/~mstiner/pdf/Stiner2004a.pdf. Retrieved 2008-09-16. 
  14. ↑ 14.0 14.1 14.2 Volume 5 of The Manners and Customs of the Ancient Egyptians: Including Their Private Life, Government, Laws, Arts, Manufacturers, Religion, Agriculture, and Early History : Derived from a Comparison of the Paintings, Sculptures, and Monuments Still Existing, with the Accounts of Ancient Author, Sir John Gardner Wilkinson, 1847
  15. ↑ 15.0 15.1 15.2 The Penny Cyclopaedia of the Society for the Difussion of Useful Knowledge, Volume 12 by Charles Knight, 1838
  16. ↑ 16.0 16.1 16.2 Zoological journal of the Linnean Society, Volume 9 1868
  17. ↑ 17.0 17.1 17.2 17.3 17.4 17.5 Cultural and Public Attitudes: Improving the Relationship between Humans and Hyaenas from Mills, M.g.L. and Hofer, H. (compilers). (1998) Hyaenas: Status Survey and Conservation Action Plan. IUCN/SSC Hyaena Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK. vi + 154 pp.
  18. ↑ 18.00 18.01 18.02 18.03 18.04 18.05 18.06 18.07 18.08 18.09 18.10 18.11 18.12 18.13 18.14 18.15 18.16 18.17 18.18 18.19 18.20 18.21 18.22 18.23 18.24 18.25 18.26 18.27 East African mammals: an atlas of evolution in Africa, Volume 3, Part 1 by Jonathan Kingdon, University of Chicago Press, 1977
  19. ↑ 19.00 19.01 19.02 19.03 19.04 19.05 19.06 19.07 19.08 19.09 19.10 19.11 19.12 19.13 19.14 19.15 19.16 19.17 19.18 19.19 19.20 19.21 19.22 19.23 19.24 19.25 19.26 19.27 19.28 19.29 19.30 19.31 19.32 19.33 19.34 19.35 19.36 19.37 19.38 19.39 19.40 19.41 19.42 19.43 19.44 Box 3.4. Common and indigenous names for the spotted hyaena from 3.4 Spotted hyaena Crocuta crocuta (Exerblen, 1777) by Heribert Hofer in Mills, M.g.L. and Hofer, H. (compilers). (1998) Hyaenas: Status Survey and Conservation Action Plan. IUCN/SSC Hyaena Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK. vi + 154 pp.
  20. ↑ Volume 1 of Sketches in Natural History: History of the Mammalia by Charles Knight, C. Cox, 1849.
  21. ↑ 21.0 21.1 Jonathan & Angela Scott (2006). Big Cat Diary: Leopard. pp. 108. ISBN 0007211813. 
  22. ↑ 22.0 22.1 22.2 22.3 22.4 22.5 Some Morphological Characteristics from Hans Kruuk’s The Spotted Hyena: A Study of Predation and Social Behaviour The University of Chicago Press, Chicago 60637, 1972.
  23. ↑ Plio-Pleistocene large carnivores from the Italian peninsula: functional morphology and macroecology by Carlo Meloro, Università degli Studi di Napoli “Federico II” Dottorato di Ricerca in Scienze della Terra Geologia del Sedimentario “XX Ciclo”, 2007.
  24. ↑ 24.0 24.1 Scavenging versus Hunting from Hans Kruuk’s The Spotted Hyena: A Study of Predation and Social Behaviour The University of Chicago Press, Chicago 60637, 1972
  25. ↑ Competition, conflict and coexistence from Cats of Africa by Luke Hunter and Gerald Hinde, Struik, 2005.
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  27. ↑ Of arcs and vaults: the biomechanics of bone-cracking in spotted hyenas (Crocuta crocuta).
  28. ↑ Marsupial has the deadliest bite by Anna Salleh, ABC News, Monday, 4 April 2005.
  29. ↑ 29.00 29.01 29.02 29.03 29.04 29.05 29.06 29.07 29.08 29.09 29.10 Social Interaction within the Clan from Hans Kruuk’s The Spotted Hyena: A Study of Predation and Social Behaviour The University of Chicago Press, Chicago 60637, 1972.
  30. ↑ The game animals of Africa by Richard Lydekker, published by London : R. Ward, limited, 1908.
  31. ↑ Communication from Hans Kruuk’s The Spotted Hyena: A Study of Predation and Social Behaviour The University of Chicago Press, Chicago 60637, 1972.
  32. ↑ 32.0 32.1 32.2 32.3 Adaptiveness and Phylogeny from Hans Kruuk’s The Spotted Hyena: A Study of Predation and Social Behaviour The University of Chicago Press, Chicago 60637, 1972.
  33. ↑ 33.0 33.1 33.2 33.3 Hunting Behaviour from Hans Kruuk’s The Spotted Hyena: A Study of Predation and Social Behaviour The University of Chicago Press, Chicago 60637, 1972
  34. ↑ Daily Activity from Hans Kruuk’s The Spotted Hyena: A Study of Predation and Social Behaviour The University of Chicago Press, Chicago 60637, 1972
  35. ↑ Solitary Hyenas Still Get the Last Laugh by Greg Soltis, LiveScience Staff, posted: 17 July 2008 04:44 pm ET
  36. ↑ 36.0 36.1 36.2 36.3 36.4 36.5 36.6 36.7 36.8 36.9 Elementary Social Behaviour Patterns from Hans Kruuk’s The Spotted Hyena: A Study of Predation and Social Behaviour The University of Chicago Press, Chicago 60637, 1972
  37. ↑ Studies Of Hyena Skull Development Put Teeth Into New Female Dominance Theory ScienceDaily (Mar. 31, 2009)
  38. ↑ Nelson,Randy J.(2005).An Introduction to Behavioral Endocrinology.Sunderland: Sinauer Associates.ISBN 0-87893-617-3
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  48. ↑ Stevenson-Hamilton 1947
  49. ↑ 49.0 49.1 Pienaar 1969
  50. ↑ Balestra 1962
  51. ↑ Deane 1962
  52. ↑ Cullen1969
  53. ↑ Bere 1966
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  55. ↑ 15TH INTERNATIONAL CAVE BEAR SYMPOSIUM SPIŠSKÁ NOVÁ VES, SLOVAKIA, 17th – 20th of September 2009
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  57. ↑ 57.0 57.1 57.2 57.3 57.4 57.5 57.6 57.7 Interactions between Hyenas and other Carnivorous Animals from Hans Kruuk’s The Spotted Hyena: A Study of Predation and Social Behaviour The University of Chicago Press, Chicago 60637, 1972
  58. ↑ 58.0 58.1 Prey preferences of the spotted hyaena (Crocuta crocuta) and degree of dietary overlap with the lion (Panthera leo) by M. W. Hayward, Terrestrial Ecology Research Unit, Department of Zoology, Nelson Mandela Metropolitan University, Eastern Cape, South Africa
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  60. ↑ Consumption from Hans Kruuk’s The Spotted Hyena: A Study of Predation and Social Behaviour The University of Chicago Press, Chicago 60637, 1972
  61. ↑ Interactions with hyenas, jackals and vultures from The Serengeti lion: a study of predator-prey relations by George B. Schaller, University of Chicago Press, 1976
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  63. ↑ Competitive interactions between spotted hyenas and lions in the Etosha National Park, Namibia by Trinkel, Martina; Kastberger, Gerald. African Journal of Ecology, Volume 43, Number 3, September 2005 , pp. 220-224(5), Blackwell Publishing
  64. ↑ Spotted Hyaena versus Brown Hyaena, Skirmishes in the Desert from Martin Harvey and M. G. L. Mills' African Predators, Smithsonian Books (Oct 2001)
  65. ↑ Hyena laughs and giggles decoded by Matt Walker, Earth News Tuesday, 30 March 2010 02:55 UK
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  67. ↑ Fosse, P. 1999. "Cave occupation during Palaeolithic times: Man and/or Hyena?," in The Role of Early Humans in the accumulation if European Lower and Middle Palaeolithic bone assemblages, Ergebnisse eines Kolloquiums, vol. 42, Monographien. Edited by S. Gaudzinski and E. Turner, pp. 73-88. Bonn: Verlag des Römisch-Germanischen Zentralmuseums.
  68. ↑ Scientist: Hyenas May Have Hunted People. Oversized Hyenas May Have Delayed Human Arrival in North America
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  70. ↑ 70.0 70.1 70.2 Preliminary data on human - carnivore conflict in Niassa National Reserve, Mozambique, particularly fatalities due to lion, spotted hyaena and crocodile, Prepared for: SGDRN (Sociedade para a Gestão e Desenvolvimento da Reserva do Niassa Moçambique) by Colleen Begg, Keith Begg, & Oscar Muemedi, June 2007
  71. ↑ Oldest Human Hair Found in Fossilized Dung Jennifer Viegas, Discovery News
  72. ↑ Spotted Hyaena from Hans Kruuk’s Hunter and hunted: relationships between carnivores and people Cambridge University Press, 2002
  73. ↑ 73.0 73.1 Knight, John (2000). Natural Enemies: People-Wildlife conflicts in Anthropological Perspective. pp. 254. ISBN 0-415-22441-1. http://www.amazon.com/Natural-Enemies-People-Wildlife-Anthropological-Anthropologists/dp/0415224411. 
  74. ↑ A Book of Man Eaters by Brigadier General R.G. Burton, Mittal Publications
  75. ↑ African Game Trails: An Account of the African Wanderings of an American Hunter, Naturalist by Theodore Roosevelt, 1909
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  77. ↑ By the Evidence, L.S.B. Leakey, Harcourt Brace Jovanovich, 1974
  78. ↑ Behaviour or Carnivores in exploited and controlled populations by Laurence G. Frank and Rosie Wooderoffe in Carnivore conservation: Volume 5 of Conservation biology series by John L. Gittleman, Cambridge University Press, 2001
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  80. ↑ Livestock predation by lions, leopards, spotted hyenas, and their vulnerability to retaliatory killing in the Maasai steppe, Tanzania from Animal Conservation, Volume 11 Issue 5, Pages 422 - 432
  81. ↑ An Account of Travels Into the Interior of Southern Africa by Sir John Barrow, published by T. Cadell, jun. and W. Davies, 1801
  82. ↑ Taming Ethiopia's hyenas by Mohammed Adow, BBC, Ethiopia
  83. ↑ Animal biography, or, Popular zoology by William Bingley, 1829
  84. ↑ Hyaenids in Captivity and Captive Breeding: Aims and Objectives from Mills, M.g.L. and Hofer, H. (compilers). (1998) Hyaenas: Status Survey and Conservation Action Plan. IUCN/SSC Hyaena Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK. vi + 154 pp.

Literature

External links