Spotted hyena

Spotted Hyena Temporal range: Late Pliocene - Recent
Conservation status
Conservation Dependent  (IUCN 2.3)
Scientific classification
Kingdom:	Animalia
Phylum:	Chordata
Class:	Mammalia
Order:	Carnivora
Family:	Hyaenidae
Genus:	Crocuta
Species:	C. crocuta
Binomial name
Crocuta crocuta (Erxleben, 1777)
File:Leefgebied gevlekte hyena.jpg
Spotted Hyena range

The Spotted Hyena, or Laughing Hyena, (Crocuta crocuta) is a carnivorous mammal of the family hyaenidae. It is the largest of the hyenas, and is native to sub-Saharan Africa, save for the Congo basin. It occurs in many different habitats, from extremely hot and arid lowland areas in its northern and southern ranges, to cold, mountainous terrains in East Africa and Ethiopia. The species can also survive near human habitations.

The species is best known for one of its vocalisations, which resembles the sound of hysterical human laughter. Though often labeled incorrectly as a scavenger, the spotted hyena is actually a powerful hunter, the majority of its nourishment being derived from live prey. The extinct Cave Hyena has been classified as subspecies of spotted hyena.

Taxonomy and evolution

The Spotted Hyena was formally described by German naturalist Johann Christian Polycarp Erxleben in 1777. The Greek root (krokoutas) of its scientific name was used by Pliny the Elder for an unknown animal, possibly the hyena, in Ethiopia. The term is derived from crocus, commonly used in the ancient world as a yellow dye. Literally, it means "the saffron-colored one".

It is thought that the ancestors of the spotted hyena branched off from the true hyenas (striped hyenas) during the Pliocene era, 5.332 million to 1.806 million years ago. As the sabre-toothed cats began to die out and be replaced by short fanged felids which were more efficient eaters, some hyenas began to hunt for themselves rather than scavenge and began evolving into new species, the modern spotted hyena being among them.

Physiology

Physical characteristics

Skeleton

Adult spotted hyenas are typically 1.3 m (4.3 ft) in length, with a shoulder height of 0.75 m (2.5 ft). Average weight ranges from 45 kg (99 lbs) for males and 55 kg (121 lbs) for females in East Africa, to more than 70 kg (154 lbs) in southern Africa. A maximum size of 90 kg (200 lbs) has been reported.

The fur's background colour is a cream to light brown, with irregular dark spots that fade with age. The muzzle is black. They have long, heavily muscled necks, lined with a coarse mane of reversed fur.

The forequarters are more heavily built than the hindquarters, giving the hyena a distinctively sloping bear-like gait. Hyenas are built for endurance, possessing a very large heart which allows them to trot at 10 km/h (6 mph) without tiring. During chases, hyenas have been clocked at running speeds of up to 50 km/h (30 mph) for over 3 km. They are good swimmers, capable of controlling their buoyancy and walking at the bottom of pools whilst holding their breath.

Hyenas have extremely strong jaws in relation to their body size. In 2005, Dr. Brady Barr of the National Geographic measured the bite forces of many different animals, including spotted hyenas for the documentary Dangerous Encounters: Bite Force. A one year old cub had a bite measured at 273 kilograms (603 pounds) of force, leading to the postulation that a full grown adult could bite at over 453 kilograms (1,000 pounds). This mandibular power, combined with its large pyramid shaped molars allows it to easily crush bone, even those of elephants. An experiment conducted in 1955 showed that the spotted hyena easily outclassed the much larger brown bear in bone crushing ability. It is often asserted in television and print that hyenas have the most powerful bite for their overall body mass when compared to other animals, although there is no scientific basis for this claim.

In the wild, the spotted hyena has an average lifespan of 12 years. It can be extended to 25 in captivity.

Reproduction

Spotted Hyena and two cubs, Ngorongoro Crater, Tanzania

The female Spotted Hyena's urogenital system is unique among mammals; the female's clitoris is elongated to form a fully erectile phallus, and the vaginal opening is at the tip of this phallus. Only the shape of the glans at the tip of the phallus makes it possible to differentiate the sexes. The female urinates, mates and gives birth through this pseudo-penis. Since it is impossible to penetrate without the female's cooperation, female hyenas have full control over whom they choose to mate with. The male hyena's penis lacks a baculum, a bone found in the genitals of most mammals.

Birth is very difficult: the internal birth canal extends almost to the subcaudal location of the vulva (which in Crocuta is fused to form a scrotum containing fatty pseudo-testes) before turning abruptly towards the clitoris, and the clitoris itself is narrow (although it ruptures with the first parturition, making subsequent births easier). 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. These factors suggests that at some point there must have been powerful selective pressures driving the evolution of masculinisation. Spotted hyenas usually have 2 cubs at a time and they are raised for about 10 months.

Researchers originally thought that one of the things that causes this characteristic of the genitals is androgens that are expressed to the fetus very early on in its development. However, it was discovered that when the androgens are held back from the fetus, the development of the female genitalia was not altered. Other hyena species lack this adaptation, making it a fairly recent one in the hyena line. Masculinised female genitalia also appears in some lemurs, spider monkeys, and the Binturong but the fused vulva is unique to the hyena.

Hyenas are born with their eyes open and teeth already fully developed after a 4 month gestation period. At birth, the cubs weigh 2.2 to 1 to 1.6 kg (1.2-3.6 lb), and are among the few mammals to commit neonatal siblicide. A same sexed litter will result in vicious fighting between the cubs, often resulting in death. This siblicide is estimated to contribute to 25% of hyena cub mortality. Since a single cub will receive more food and mature faster, this behavior is probably adaptive. Spotted hyena milk is very rich, having the highest protein content (14.9%) of any terrestrial carnivore, and 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. Two to six weeks after whelping, young are transported to the communal den. Young depend entirely on milk for about 8 months and are not weaned until 12 to 16 months old. Maturation is at three years, females later than males. Female offspring remain in their natal clan while males leave at around two years.

Behaviour

Spotted hyenas mark their territories by excreting an oily, yellow substance from their anal glands onto surrounding bushes and grass. To do this, the anal pouch is turned inside out, or everted. The anal glands are everted also as a submissive posture to dominant hyenas. Scent marking is also done by scraping the ground with the paws, which deposits scent from glands on the bottoms of the feet.

Group organization

Young Spotted Hyenas rest on a road in the Kruger National Park in South Africa

Studies strongly suggest convergent evolution in hyena and primate intelligence. Spotted hyena societies are more complex than those of other carnivorous mammals, and have been reported to be remarkably similar to those cercopithecine primates in respect to group size, structure, competition and cooperation. Like primates, spotted hyenas use multiple sensory modalities, recognise individual conspecifics, they are conscious that some clan-mates may be more reliable than others, they 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. Compared to other hyenas, spotted hyenas show a greater relative amount of frontal cortex exclusive to motor control functions. Spotted hyenas frequently deposit their droppings in "latrines" which are usually situated at clan boundraries.

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 . Clan life is centered around a communal den, however only cubs live within the den itself. Each clan is permanent social group called a fission-fusion society. A complicated social hierarchy governs the clan, which cubs often learn before they begin to walk. Females are the dominant members, followed in rank by cubs, while adult males rank lower than the lowest ranking female, the fully matured males form the lowest ranking group throughout the clan. The society is highly structured, with dominance relationship between the matrilines (the groups of females descended from a single mother) that endure for generations. Social behavior is very complex, involving frequent alliances and shifting social ties. In this hyenas are more similar to many old world primates than they are to other social carnivores. Male hyenas, which are usually smaller and less aggressive than females, often leave the clan when they are about two years old, while females stay within their birth clan.

Subordinate members of the clan lick the pseudo-penis of a higher ranked female as a sign of submission. The matriarch's pseudo-penis is licked by all members of the clan, while male's penises are rarely licked because the highest ranked male is subordinate to the lowest ranked female.

Females tend to mate with males from other clans, thereby preventing inbreeding. Female hyenas very rarely mate with highly aggressive males. Instead, calmer and more docile males are selected. Patience is especially important since courtship can last as long as a year. For this reason, dominant and impatient males have difficulty finding mates. Despite the complicated courtship, the female raises her pups without the male. Infanticide is common. "Prior to the mother's return, another adult female (a full sister to the new mother) arrived and methodically killed both newborns with crushing bites to the head" (Paula A. White)

Hyenas within the same clan rarely fight in a way that can damage them seriously. Most bickering is settled quickly, even by members that have similar ranking in the social hierarchy. Some loud noises and a couple of light bites is usually enough, and if the fight ever gets out of hand, it is quite normal for a hyena of a higher rank to step in and interrupt the fight.

Even hyenas that are strangers to each other would rather avoid battle than recklessly try to kill each other. Usually, scent marking territories avoids conflicts: if a lone hyena should enter a hostile territory anyway, it keeps a low profile and stays near the borders. Female hyenas are treated with more hostility than males, since males from different clans are needed for breeding in the clan. Strangers are rarely accepted in a clan, but if so, they are usually placed at the bottom of the ranking system. When large scale confrontations do occur (with lions or other hyena clans), hyena form a distinctive "wall" by standing shoulder to shoulder and advancing on the threat as a group.

Like many social carnivores, spotted hyenas are playful, especially when young. In captivity they can become very tame, and both native Africans and Europeans living in Africa have sometimes successfully made pets of them.

Hunting and diet

Spotted hyenas feed from a giraffe carcass amongst a large number of vultures

Although spotted hyenas are better adapted to a scavenging lifestyle than any other predators in their range, they obtain the majority of their nourishment through hunting. Their teeth are not as specialised to a solely scavenging lifestyle like the striped and brown hyenas, having further developed them to be more "all purpose". Spotted hyenas tend to target medium-sized ungulates such as wildebeest or zebra, rather than larger ones such as cape buffalo or smaller ones such as Thomson's gazelle. Unlike wolves, spotted hyenas rely more on sight than smell in selecting prey. They will readily chase after prey that retreats in deep water. Like African wild dogs, spotted hyenas chase their prey over long distances, until the selected quarry exhausts itself. Because of their hunting methods, spotted hyenas are typically more likely to select the physically least able of a herd. When attacking large prey, they bite the animal's hind quarters and tear open the abdomen. The entrails and leg muscles are usually eaten first. If the victim is a pregnant female, then the fetus is among the first things to be eaten. The head is always left last. Spotted hyenas can consume at least 14.5 kg at a meal, up to a third of their own body weight, which is an exceptionally high figure for mammals. They have a very powerful digestive system with highly acidic fluids. This makes them capable of eating and digesting their entire prey, including skin, teeth, horns, bones and even hooves. This results in them having crusty white droppings, due to the amount of calcium they ingest. The spotted hyena's digestive system is so efficient, it can even derive nourishment from mummified corpses. There are reports of hyenas entering campsites and consuming aluminium pots and pans. Indigestible parts are vomited in the form of pellets. In areas with high spotted hyena densities, discarded bones are rarely found except during the wildebeest calving season when some hyenas consume so much, that they only eat the choiciest parts of their prey. When eating together, spotted hyenas compete with one another through speed of eating rather than fighting. One pack was recorded to have completely consumed an adult zebra in 36 minutes. Rare accounts of surplus killing have been reported, one example being in 1966, in which during one storm ridden night, a group of hyenas killed 110 Thomson's gazelle and ate only a small proportion of the victims.

Spotted hyenas 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. Though hyenas commonly hunt in packs, a single hyena is sometimes sufficient to kill an adult bull wildebeest. Zebras require different hunting methods to those used for wildebeest, due to their habit of running in tight groups and aggressive defence from stallions. Typical zebra hunting groups consist of 10-25 hyenas who indulge in activities such as scent marking before setting off. 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 themselves 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. Spotted hyenas rarely attack cape buffalo, due to differences in habitat preferences, though hyenas have been recorded to kill fully grown bulls. Other recorded prey items include fish, tortoises, black rhino, hippo calves, elephant calves, pangolins, pythons, jackals, lions, livestock, dogs and humans.

Spotted hyenas tend to scavenge more in daylight hours, thus facilitating the spotting of alighting vultures, to which they react quicker than most other carnivores. They are more likely to stay near a lion kill or human settlement than any other African predators except jackals. Spotted hyenas will sometimes cache food for later consumption. Some spotted hyenas have been reported to store food underwater. Spotted hyenas consume very little water, usually spending no more than 30 seconds drinking.

Interspecific predatory relationships

The relationship between hyenas and lions in areas where they coexist is unique in its complexity and intensity. Lions and hyenas are both apex predators which feed on the same prey, and are therefore in direct competition with one other. As such, they will often fight over and steal each others' kills. Though it is popularly assumed that hyenas are opportunistic scavengers which profit from the lion's hunting abilities, it is quite often the case that the reversal is true. In Tanzania's Ngorongoro Crater, the hyena population greatly exceeds that of the resident lions, which obtain a large proportion of their food by pirating hyena prey. The feud between the two species does however seem to encompass more than just battles over food. In the animal kingdom, the territorial boundaries of another species are usually disregarded. Hyenas and lions are an exception to this seeing as they set boundaries against each other as they would against members of their same species. Male lions are extremely aggressive toward hyenas, and have been observed to hunt and kill hyenas without eating them. Conversely, hyenas are major predators of lion cubs. When attacking adults, hyenas go after groups of females or better yet, a single female. However, healthy adult males, even single ones, are generally avoided.

Spotted hyenas typically dominate solitary felines like leopards and cheetahs. Although the diet of leopards and cheetahs shows little overlap with that of hyenas, hyenas will often follow the cats in an attempt at stealing their kills. A single hyena is usually sufficient at driving a leopard or cheetah from its kill, though some male leopards have been recorded to occasionally kill hyenas for food.

In areas where spotted hyenas and African wild dogs are sympatric, the former often trail wild dog packs in order to steal their kills. Hyenas have been shown to be attracted to large numbers of wild dogs, even when no kill is present. Though adult hyenas physically outmatch wild dogs, a pack of wild dogs can hold its own against a group of hyenas due to their habit of working more in unison.

Vocalizations

The spotted hyena is among the most vocal African mammals, with over 11 different sounds being recorded.

• Groans/soft squeals – Often exchanged during greeting.
• Whoop – A contact call, varying in pitch and intensity. A fast whoop is a rallying cry given by excited hyenas during conflict or at a kill site. Apparently, calls emitted by males are usually ignored. Calls emitted by females however are responded to immediately.
• Lowing – A sound made by impatient hyenas, usually when waiting for their turn at a kill.
• Grunting – A very low growl with the mouth closed that accompanies aggressive behaviour.
• Growling – A deep, resonating rumble made by defensive hyenas threatening to bite.
• Rattling growl – A low-pitched, soft, staccato grunt given as an alarm call.
• Giggling – A high pitched, cackling laugh, typically emitted by hyena being chased; expresses intense fear.
• Yelling – A roaring scream voiced by hyenas attempting to escape attackers.

Body language

• Phallic inspection – An affectionate greeting ceremony between clan members, usually initiated by lower ranking individuals. After mutually sniffing the nose, mouth, head, and neck, the 2 hyenas stand head-to-tail and sniff/touch each others extended phallus for up to 1/2 minutes with their back legs cocked. This greeting is performed by both sexes at the age of one month onwards. Adult males rarely greet with females in this manner.
• Social grooming – Licking and nibble-grooming between mothers and offspring, though rarely between adults.
• Courtship – The male approaches the female from behind with his head bowed and penis extended. He will paw the ground behind her, depositing his scent with his toe glands.

Relationships with humans

Historical perceptions

The Ancient Greek philosopher Aristotle was noted to have first challenged the condemnations directed toward the hyena's supposed hermaphroditism. It is however doubtful he had any first hand experience with spotted hyenas to begin with, considering his physical descriptions match those of the striped hyena which does not share its spotted cousin's sexual anomalies.

Through the early days of the Christian era to the end of the Middle Ages, hyenas were thought to annually change sex and habitually rob graves. The former charge was traditionally linked to the Jews. Sir Walter Raleigh, in his 1614 History of the World believed that hyenas were not present in Noah's Ark, as he believed them to be mixed animals like mules, and thus could easily be recreated.

1656 was the year of the first predator culling legislation in South Africa. The hyena was known as "wolf", and rewards of up to four realen were given to those who managed to kill them. Predator culling was a common practice in the early African game reserves until the mid 20th century. In the Kruger National Park between 1903 and 1927, 18,428 predators were killed in an effort to protect game herds. Spotted hyenas accounted for 521 of the killed predators.

In African folklore

Spotted hyenas vary in their folkloric and mythological depictions, depending on the ethnic group from which the tales originate. 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. 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. Belief in "werehyenas" is so entrenched within the traditional lore of the Bornu people of north-eastern Nigeria, that their language even contains a special word bultungin which translates as "I change myself into a hyena".

Attacks on humans

While hyenas, in general, do not hunt humans, some attacks occurred and even caused human death. 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.

References

• Template:IUCN2006
• Androgens and the Role of Female "Hyperaggressiveness" in Spotted Hyenas (Crocuta crocuta) Wolfgang Goymann, Marion L. East, and Heribert Hofer (pdf) - 'Androgen-independent mechanisms are likely to also play an important role, as treatment with anti-androgens during fetal development did not produce females without a pseudo-penis (Drea, Weldele, Forger, Coscia, Frank, Licht, and Glickman, 1998).'
• [http://www.current-biology.com/content/article/fulltext?uid=PIIS0960982206023165

External links

• http://hyenas.zoology.msu.edu/ The research of Dr. Kay Holekamp and her students at Michigan State University focuses on mammalian behavioral development and its physiological substrates; investigating how social, ecological, and endocrine variables interact during an individual's early development to influence its subsequent behavior and its reproductive success as an adult.
• http://msuhyenas.blogspot.com/ MSU Hyena Blog for general audience containing narrative and photos of ongoing hyena research and activities in Masai Mara, Kenya. Blog was started Aug 2008
• The IUCN Hyaenidae Specialist Group page on spotted hyena.
• Quirks & Quarks (science radio program)