The spotted hyena (Crocuta crocuta), also known as the laughing hyena, is a hyena species, currently classed as the sole extant member of the genus Crocuta, native to sub-Saharan Africa. It is listed as being of least concern by the IUCN due to its widespread range and large numbers estimated between 27,000 and 47,000 individuals. The species is, however, experiencing declines outside of protected areas due to habitat loss and poaching. Populations of Crocuta, usually considered a subspecies of Crocuta crocuta, known as cave hyenas, roamed across Eurasia for at least one million years until the end of the Late Pleistocene. The spotted hyena is the largest extant member of the Hyaenidae, and is further physically distinguished from other species by its vaguely bear-like build, rounded ears, less prominent mane, spotted pelt, more dual-purposed dentition, fewer nipples, and pseudo-penis. It is the only placental mammalian species where females have a pseudo-penis and lack an external vaginal opening. The spotted hyena is the most social of the Carnivora in that it has the largest group sizes and most complex social behaviours. Its social organisation is unlike that of any other carnivore, bearing closer resemblance to that of cercopithecine primates (baboons and macaques) with respect to group size, hierarchical structure, and frequency of social interaction among both kin and unrelated group-mates. The social system of the spotted hyena is openly competitive, with access to kills, mating opportunities and the time of dispersal for males depending on the ability to dominate other clan-members and form ally networks. Females provide only for their own cubs rather than assist each other, and males display no paternal care. However, the spotted hyena is also very cooperative with their clan-mates; often hunting, eating, and resting together, and making use of their numeracy and communication skills to fight off a common enemy. Spotted hyena society is matriarchal; females are larger than males and dominate them. The spotted hyena is a highly successful animal, being the most common large carnivore in Africa. Its success is due in part to its adaptability and opportunism; it is primarily a hunter but may also scavenge, with the capacity to eat and digest skin, bone and other animal waste. In functional terms, the spotted hyena makes the most efficient use of animal matter of all African carnivores. The spotted hyena displays greater plasticity in its hunting and foraging behaviour than other African carnivores; it hunts alone, in small parties of 2–5 individuals, or in large groups. During a hunt, spotted hyenas often run through ungulate herds to select an individual to attack. Once selected, their prey is chased over a long distance, often several kilometres, at speeds of up to 60 kilometres per hour (37 mph). The spotted hyena has a long history of interaction with humanity; depictions of the species exist from the Upper Paleolithic period, with carvings and paintings from the Lascaux and Chauvet Caves. The species has a largely negative reputation in both Western culture and African folklore. In the former, the species is mostly regarded as ugly and cowardly, while in the latter, it is viewed as greedy, gluttonous, stupid, and foolish, yet powerful and potentially dangerous. The majority of Western perceptions on the species can be found in the writings of Aristotle and Pliny the Elder, though in relatively unjudgmental form. Explicit, negative judgments occur in the Physiologus, where the animal is depicted as a hermaphrodite and grave-robber. The IUCN's hyena specialist group identifies the spotted hyena's negative reputation as detrimental to the species' continued survival, both in captivity and the wild.
Etymology and naming The spotted hyena's scientific name Crocuta was once widely thought to be derived from the Latin loanword crocutus, which translates as 'saffron-coloured one', in reference to the animal's fur colour. This was proven to be incorrect, as the correct spelling of the loanword would have been Crocāta, and the word was never used in that sense by Graeco-Roman sources. Crocuta actually comes from the Ancient Greek word Κροκόττας (krokottas), which is derived from the Sanskrit koṭṭhâraka, which in turn originates from kroshṭuka (both of which were originally meant to signify the golden jackal). The earliest recorded mention of Κροκόττας is from Strabo's Geographica, where the animal is described as a mix of wolf and dog native to Ethiopia.
From Classical antiquity until the Renaissance, the spotted and striped hyena were either assumed to be the same species, or distinguished purely on geographical, rather than physical, grounds. Hiob Ludolf, in his Historia aethiopica, was the first to clearly distinguish the Crocuta from Hyaena as different animals, though he never had any first hand experience of the species, having gotten his accounts from an Ethiopian intermediary. Confusion still persisted over the exact taxonomic nature of the hyena family in general, with most European travelers in Ethiopia referring to hyenas as "wolves". This partly stems from the Amharic word for hyena, ጅብ (jɨbb), which is linked to the Arabic word ذئب (dhiʾb) 'wolf'. The first detailed first-hand descriptions of the spotted hyena by Europeans come from Willem Bosman and Peter Kolbe. Bosman, a Dutch tradesman who worked for the Dutch West India Company at the Gold Coast (modern-day Ghana) from 1688 to 1701, wrote of Jakhals, of Boshond (jackals or woodland dogs) whose physical descriptions match the spotted hyena. Kolben, a German mathematician and astronomer who worked for the Dutch East India Company in the Cape of Good Hope from 1705 to 1713, described the spotted hyena in great detail, but referred to it as a "tigerwolf", because the settlers in southern Africa did not know of hyenas, and thus labelled them as "wolves". Bosman and Kolben's descriptions went largely unnoticed until 1771, when the Welsh naturalist Thomas Pennant used the descriptions and his personal experience with a captive specimen as a basis for consistently differentiating the spotted hyena from the striped in his Synopsis of Quadrupeds. The description given by Pennant was precise enough to be included by Johann Erxleben in his Systema regni animalis by simply translating Pennant's text into Latin. Crocuta was finally recognised as a separate genus from Hyaena in 1828.
Taxonomy, origins and evolution
Unlike the striped hyena, for which a number of subspecies were proposed in light of its extensive modern range, the spotted hyena is a genuinely variable species, both temporally and spatially. Its range once encompassed almost all of Africa and Eurasia, and displayed a large degree of morphological geographic variation, which led to an equally extensive set of specific and subspecific epithets. It was gradually realised that all of this variation could be applied to individual differences in a single subspecies. In 1939, biologist L Harrison Matthews demonstrated through comparisons between a large selection of spotted hyena skulls from Tanzania that all the variation seen in the then recognised subspecies could also be found in a single population, with the only set of characters standing out being pelage (which is subject to a high degree of individual variation) and size (which is subject to Bergmann's Rule). When fossils are taken into consideration, the species displayed even greater variation than it does in modern times, and a number of these named fossil species have since been classed as synonymous with Crocuta crocuta, with firm evidence of there being more than one species within the genus Crocuta still lacking.
The ancestors of the genus Crocuta diverged from Hyaena (the genus of striped and brown hyenas) 10 million years ago. The ancestors of the spotted hyena probably developed social behaviours in response to increased pressure from other predators on carcasses, which forced them to operate in teams. Sociality has been correlated with the volume of the anterior cerebrums, and fossil evidence of other Crocuta species closely related to the spotted hyena has shown that they began forming clans and becoming social approximately 350,000 years ago. At one point in their evolution, spotted hyenas developed sharp carnassials behind their crushing premolars; this rendered waiting for their prey to die no longer a necessity, as is the case for brown and striped hyenas, and thus they 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 land. It has been theorised that female dominance in spotted hyena clans could be an adaptation in order to successfully compete with males on kills, and thus ensure that enough milk is produced for their cubs. Another theory is that it is an adaptation to the length of time it takes for cubs to develop their massive skulls and jaws, thus necessitating greater attention and dominating behaviours from females. Both Björn Kurtén and Camille Arambourg promoted an Asiatic origin for the species; Kurtén focussed his arguments on the Plio-Pleistocene taxon Crocuta sivalensis from the Siwaliks, a view defended by Arambourg, who nonetheless allowed the possibility of an Indo-Ethiopian origin. This stance was contested by Ficarelli and Torre, who referred to evidence of the spotted hyena's presence from African deposits dating from the early Pleistocene, a similar age to the Asian C. sivalensis. Modern scholarship supports an African origin for the genus, with the earliest fossils of the genus Crocuta dating to the early Pliocene of Africa, around 3.63 to 3.85 million years ago. The earliest known fossil record of Crocuta crocuta in Africa is from the Cradle of Humankind, specifically from the Sterkfontein Member 4 which is dated approximately 2.1 million years ago in minimum, and it is also common in deposits dated between 2 to 1.5 million years ago. Analysis of the mitochondrial genomes of Eurasian Crocuta (cave hyena) specimens shows no clear separation from African lineages. It also suggests that modern spotted hyena populations descend from a widely ranging Afro-Eurasian population that was only recently reduced in range to Africa exclusively. However, analysis of the full nuclear genome suggests that Late Pleistocene African and Eurasian Crocuta populations were largely separate, having estimated to have diverged from each other around 2.5 million years ago, closely corresponding to the age of the earliest Crocuta specimens in Eurasia, which are around 2 million years ago from China. The nuclear genome results also suggest that the European and Asian populations were distinct from each other, but were more closely related to each other overall than to African Crocuta populations. Analysis of the nuclear genome suggests that there had been interbreeding between African and Eurasian populations for some time after the split, which likely explains the discordance between the nuclear and mitochondrial genome results, with the mitochondrial genomes of African and European Crocuta more closely related to each other than to Asian Crocuta, suggesting gene flow between the two groups after the split between the Asian and European populations. Its appearance in Europe and China coincided with the decline and eventual extinction of Pachycrocuta brevirostris, the giant short-faced hyena. As there is no evidence of environmental change being responsible, it is likely that the giant short-faced hyena became extinct due to competition with the spotted hyena. However, more recent analysis found Crocuta likely didn't play a role in the extinction of Pachycrocuta in Europe due to the lack of temporal overlap.
Description
Anatomy
The spotted hyena has a strong and well-developed neck and forequarters, but relatively underdeveloped hindquarters. The rump is rounded rather than angular, which prevents attackers coming from behind from getting a firm grip on it. The head is wide and flat with a blunt muzzle and broad rhinarium. In contrast to the striped hyena, the ears of the spotted hyena are rounded rather than pointed. Each foot has four digits, which are webbed and have short, stout and blunt claws. The paw-pads are broad and flat, with the whole undersurface of the foot around them being naked. The tail is relatively short, being 300–350 mm (12–14 in) long, and resembles a pompom in appearance. Unusually among hyaenids, and mammals in general, the female spotted hyena is considerably larger than the male. Both sexes have a pair of anal glands which open into the rectum just inside the anal opening. These glands produce a white, creamy secretion which is pasted onto grass stalks by everting the rectum. The odour of this secretion is strong, smelling of boiling cheap soap or burning, and can be detected by humans several metres downwind. The spotted hyena has a proportionately large heart, constituting close to 1% of its body weight, thus giving it great endurance in long chases. In contrast, a lion's heart makes up only 0.45–0.57 percent of its body weight. The now extinct Eurasian populations were distinguished from the modern African populations by their shorter distal extremities and longer humerus and femur.
The skull of the spotted hyena differs from that of the striped hyena by its much greater size and narrower sagittal crest. For its size, the spotted hyena has one of the most powerfully built skulls among the Carnivora. The 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. The spotted hyena also has its carnassials situated behind its bone-crushing premolars, the position of which allows it to crush bone with its premolars without blunting the carnassials. Combined with large jaw muscles and a special vaulting to protect the skull against large forces, these characteristics give the spotted hyena a powerful bite which can exert a pressure of 80 kgf/cm2 (1140 lbf/in²), which is 40% more force than a leopard can generate. The jaws of the spotted hyena outmatch those of the brown bear in bone-crushing ability, and free ranging hyenas have been observed to crack open the long bones of giraffes measuring 7 cm in diameter. A 63.1 kg (139 lb) spotted hyena is estimated to have a bite force of 565.7 newtons at the canine tip and 985.5 newtons at the carnassial Eocene. One individual in a study was found to exert a bite force of 4,500 newtons on the measuring instruments.
Dimensions The spotted hyena is the largest extant member of the Hyaenidae. Adults measure 95–165.8 cm (37.4–65.3 in) in body length, and have a shoulder height of 70–91.5 cm (27.6–36.0 in). Adult male spotted hyenas in the Serengeti weigh 40.5–55.0 kg (89.3–121.3 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). Exceptionally large weights of 81.7 kg (180 lb) and 90 kg (200 lb) are known. It has been estimated that adult members of the now extinct Eurasian populations weighed 102 kg (225 lb).
Fur Fur colour varies greatly and changes with age. Unlike the fur of the striped and brown hyena, that of the spotted hyena consists of spots rather than stripes and is much shorter, lacking the well defined spinal mane of the former two species. The base colour generally is a pale greyish-brown or yellowish-grey on which an irregular pattern of roundish spots is superimposed on the back and hind quarters. The spots, which are of variable distinction, may be reddish, deep brown or almost blackish. The spots vary in size, even on single individuals, but are commonly 20 mm (0.79 in) in diameter. A less distinct spot pattern is present on the legs and belly but not on the throat and chest. Some research groups (such as Ngorongoro Crater Hyena Project and MSU Hyena Project) often use the spot patterns to help identify individual hyenas. A set of five, pale and barely distinct bands replace the spots on the back and sides of the neck. A broad, medial band is present on the back of the neck, and is lengthened into a forward facing crest. The crest is mostly reddish-brown in colour. The crown and upper part of the face is brownish, save for a white band above both eyes, though the front of the eyes, the area around the rhinarium, the lips and the back portion of the chin are all blackish. The limbs are spotted, though the feet vary in colour, from light brown to blackish. The fur is relatively sparse and consists of two hair types; moderately fine underfur (measuring 15–20 mm (0.59–0.79 in)) and long, stout bristle hairs (30–40 mm (1.2–1.6 in)). European Paleolithic rock art depicting the species indicates that the Eurasian populations retained the spots of their modern-day African counterparts.
Female genitalia
The genitalia of the female closely resembles that of the male; the clitoris is shaped and positioned like a penis, a pseudo-penis, and is capable of erection. The female also possesses no external vagina (vaginal opening), as the labia are fused to form a pseudo-scrotum. The pseudo-penis is traversed to its tip by a central urogenital canal, through which the female urinates, copulates and gives birth. The pseudo-penis can be distinguished from the males' genitalia by its somewhat shorter length, greater thickness, and more rounded glans. In both males and females, the base of the glans is covered with penile spines. The formation of the pseudo-penis appears largely androgen independent, as the pseudo-penis appears in the female fetus before differentiation of the fetal ovary and adrenal gland. When flaccid, the pseudo-penis is retracted into the abdomen, and only the prepuce is visible. After giving birth, the pseudo-penis is stretched, and loses many of its original aspects; it becomes a slack-walled and reduced prepuce with an enlarged orifice with split lips.
Behaviour
Social behaviour Spotted hyenas are social animals that live in large communities (referred to as "clans") which can consist of at most 80 individuals. Group-size varies geographically; in the Serengeti, where prey is migratory, clans are smaller than those in the Ngorongoro Crater, where prey is sedentary. Spotted hyena clans are more compact and unified than wolf packs, but are not as closely knit as those of African wild dogs. Females usually dominate males, including in cases where low-ranking females generally dominate over high-ranking males, but they will also occasionally co-dominate with a male. There have also been cases in which a clan has been led by a male rather than a female. Cubs inherit the social rank of their mother and mirror the social associations she has with other clan members, and cubs can maintain these social associations with other clan members long after dependence on their mother. So when the matriarch passes away (or, in rare instances, disperses into another clan), their female cubs have the rank and social support by other clan members to become the new matriarch. It is typical for females to remain with their natal clan, thus large clans usually contain several matrilines, whereas males typically disperse from their natal clan at the age of 2½ years. When a male co-dominates with a female or is otherwise able to lead, this is because the male was born to the matriarch of the clan and has taken the rank directly below his mother.
The clan is a fission–fusion society, in which clan-members do not often remain together, but may forage in small groups. High-ranking hyenas maintain their position through aggression directed against lower-ranking clan-members. Spotted hyena hierarchy is nepotistic; the offspring of dominant females automatically outrank adult females subordinate to their mother. However, rank in spotted hyena cubs is greatly dependent on the presence of the mother; low-ranking adults may act aggressively toward higher-ranking cubs when the mother is absent. Although individual spotted hyenas only care for their own young, and males take no part in raising their young, cubs are able to identify relatives as distantly related as great-aunts. Also, males associate more closely with their own daughters rather than unrelated cubs, and the latter favor their fathers by acting less aggressively toward them. Spotted hyena societies are more complex than those of other carnivorous mammals, and are remarkably similar to those of cercopithecine primates in respect to group size, structure, competition and cooperation. Like cercopithecine primates, spotted hyenas use multiple sensory modalities, recognise individual conspecifics, are conscious that some clan-mates may be more reliable than others, recognise third-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. In this latter trait, the spotted hyena further show parallels with primates by acquiring rank through coalition. However, rank reversals and overthrows in spotted hyena clans are rare. When changes in rank do occur, the long-term effects may be profound: Spotted hyenas that underperform their inherited ranks in their formative months are about 1.5 times more likely to die at any given point than are hyenas that maintain or surpass their own inherited ranks. The social network dynamics of spotted hyenas are determined by multiple factors. Environmental factors include rainfall and prey abundance; individual factors include preference to bond with females and with kin; and topological effects include the tendency to close triads in the network. Female hyenas are more flexible than males in their social bonding preferences. Higher ranking adult spotted hyenas tend to have higher telomere length and higher levels of some immune defense proteins in their blood serum. Territory size is highly variable, ranging from less than 40 km2 (15 sq mi) in the Ngorongoro Crater to over 1,000 km2 (390 sq mi) in the Kalahari. Home ranges are defended through vocal displays, scent marking and boundary patrols. Clans mark their territories by either pasting or pawing in special latrines located on clan range boundaries. Spotted hyenas use scent gland secretions to distinguish between members of their own clan and members of neighboring clans. Within the same clan, differences in scent gland compositions can help individuals differentiate the reproductive states and sex of their members. One study analyzed the scent gland secretions of several hyenas belonging to three different clans and discovered a high degree of similarity in fatty acid composition among members of the same clans, while hyenas of different clans had more dissimilar scent gland secretions. Further studies have proposed a symbiotic relationship between spotted hyenas and their scent gland bacteria, where the differences in fatty acids can be attributed to fermentation by different microbes. Clan boundaries are usually respected; hyenas chasing prey have been observed to stop dead in their tracks once their prey crosses into another clan's range. Hyenas will however ignore clan boundaries in times of food shortage. Males are more likely to enter another clan's territory than females are, as they are less attached to their natal group and will leave it when in search of a mate. Hyenas travelling in another clan's home range typically exhibit bodily postures associated with fear, particularly when meeting other hyenas. An intruder can be accepted into another clan after a long period of time if it persists in wandering into the clan's territory, dens or kills.
Mating, reproduction, and development
The spotted hyena is a non-seasonal breeder, though a birth peak does occur during the wet season. Females are polyestrous, with an estrus period lasting two weeks. Like many feliform species, the spotted hyena is promiscuous, and no enduring pair bonds are formed. Members of both sexes may copulate with several mates over the course of several years. Males will show submissive behaviour when approaching females in heat, even if the male outweighs his partner. Females usually favour younger males born 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. Passive males tend to have greater success in courting females than aggressive ones. Copulation in spotted hyenas is a relatively short affair, lasting 4–12 minutes, and typically only occurs at night with no other hyenas present. The mating process is complicated, as the male's penis enters and exits the female's reproductive tract through her pseudo-penis rather than directly through the vagina, which is blocked by the false scrotum and testes. These unusual traits make mating more laborious for the male than in other mammals, and also make forced copulation physically impossible. The female retracts her clitoris before the male's penis enters it by sliding beneath it, an operation facilitated by the penis's upward angle. The hyenas then adopt a typical mammalian mating posture and usually lick their genitals for several minutes after mating. Copulation may be repeated multiple times during a period of several hours.
The length of the gestation period tends to vary greatly, but the average length is 110 days. 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. 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. The molecular mechanism behind this may be that spotted hyenas have a much lower concentration of sex hormone-binding globulin than other hyena species, resulting in increased exposure of genitalia and the central nervous system to sex steroids. The average litter consists of two cubs, with three occasionally being reported. Males take no part in the raising of young. Giving birth is difficult for female hyenas, as the females give birth through their narrow clitoris, and spotted hyena cubs are the largest carnivoran young relative to their mothers' weight. During parturition, the clitoris ruptures to facilitate the passage of the young, and may take weeks to heal. Cubs are born with soft, dark brown hair, and weigh 1.5 kg (3.3 lb) on average. Unique among carnivorous mammals, spotted hyenas are also born with their eyes open and with 6–7 mm (0.24–0.28 in)-long canine teeth and 4 mm (0.16 in)-long incisors. Also, cubs will attack each other shortly after birth. This is particularly apparent in same sexed litters, and can result in the death of the weaker cub. This neonatal siblicide kills an estimated 25% of all hyenas in their first month. Male cubs which survive grow faster and are likelier to achieve reproductive dominance, while female survivors eliminate rivals for dominance in their natal clan. Lactating females can carry 3–4 kg (6.6–8.8 lb) of milk in their udders. Spotted hyena milk has the highest protein and fat content of any terrestrial carnivore. Cubs will nurse from their mother for 12–16 months, though they can process solid food as early as three months. Mothers do not regurgitate food for their young. Females are protective of their cubs, and will not tolerate other adults, particularly males, approaching them. Spotted hyenas exhibit adult behaviours 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 2–3 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. Spotted hyenas reach sexual maturity at the age of three years. The average lifespan in zoos is 12 years, with a maximum of 25 years.
Denning behaviour
The clan's social life revolves around a communal den. While some clans may use particular den sites for years, others may use several different dens within a year or several den sites simultaneously. Spotted hyena dens can have more than a dozen entrances, and are mostly located on flat ground. The tunnels are usually oval in section, being wider than they are high, and narrow down from an entrance width of ½–1 metre (1.6–7.7 ft) to as small as 25 cm (9.8 in). In the rocky areas of East Africa and Congo, spotted hyenas use caves as dens, while those in the Serengeti use kopjes as resting areas in daylight hours. Dens have large bare patches around their entrances, where hyenas move or lie down on. Because of their size, adult hyenas are incapable of using the full extent of their burrows, as most tunnels are dug by cubs or smaller animals. The structure of the den, consisting of small underground channels, is likely an effective anti-predator device which protects cubs from predation during the absence of the mother. Spotted hyenas rarely dig their own dens, having been observed for the most part to use the abandoned burrows of warthogs, springhares and jackals. Faeces are usually deposited 20 metres (66 feet) away from the den, though they urinate wherever they happen to be. Dens are used mostly by several females at once, and it is not uncommon to see up to 20 cubs at a single site. The general form of a spotted hyena den is tunnel-shaped, with a spacious end chamber used for sleeping or breeding. This chamber measures up to 2 metres (6.6 feet) in width, the height being rather less. Females generally give birth at the communal den or a private birth den. The latter is primarily used by low status females to maintain continual access to their cubs, as well as ensure that they become acquainted with their cubs before transferral to the communal den.
Intelligence Compared to other hyenas, the spotted hyena shows a greater relative amount of frontal cortex which is involved in the mediation of social behavior. Studies strongly suggest convergent evolution in spotted hyena and primate intelligence. 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. The intelligence of the spotted hyena was attested to by Dutch colonists in 19th-century South Africa, who noted that hyenas were exceedingly cunning and suspicious, particularly after successfully escaping from traps. Spotted hyenas seem to plan on hunting specific species in advance; hyenas have been observed to engage in activities such as scent marking before setting off to hunt zebras, a behaviour which does not occur when they target other prey species. One of the signs of social intelligence is the ability to have a keen olfactory sense or nasal recognition. Spotted hyenas have unique scent signatures that help them distinguish themselves from other clans and/or individuals (i.e., males or females conspecific), which enables them to mark their territories with secretions from their scent glands. Also, spotted hyenas have been recorded to utilise deceptive behaviour, including giving alarm calls during feeding when no enemies are present, thus frightening off other hyenas and allowing them to temporarily eat in peace. Similarly, mothers will emit alarm calls when attempting to interrupt attacks on their cubs by other hyenas.
Responses to stress Spotted hyenas are a good subject for studying the causes and consequences of stress because of the behavioral plasticity they exhibit to respond to their variable and unpredictable environment. The hormonal and behavioral responses of spotted hyenas to a variety of stressful stimuli can shed light on how they will adapt in the future and how other gregarious, group-living species may respond to similar stressors. Stress responses are often measured using corticosteroid levels non-invasively in hyenas, through the analysis of fecal or salivary glucocorticoid samples. While corticosteroids typically fluctuate in predictable patterns across life-history states, spotted hyenas exhibit hormonal and corresponding behavioral responses to unpredictable social, environmental, and anthropogenic stressors. Social stress Aggression, social stability, and social connectedness play an important role in reinforcing hierarchies in spotted hyena clans, and social interactions can modulate stress levels. In particular, being the target of aggression or experiencing social instability impose stress on spotted hyenas. Exhibiting aggression, or experiencing social connectedness as juveniles can both immediately decrease stress, and reduce stress during later-life stages. Environmental stress Reductions in food and available foraging environments cause significant stress in wild spotted hyenas. These challenges are exacerbated by the increased unpredictability of migratory patterns in hyena prey resulting from climate related changes in the lengths of wet and dry seasons. Spotted hyenas are responding by foraging over longer distances, which increases energy expenditure, and consequently the stress associated with lactation for nursing females. Increased foraging range also invokes social stress from encroaching on other hyena clans' territories in search of prey. Anthropogenic stress While spotted hyenas typically show a range of innovative behavior, such as hiding in vegetative cover to avoid cattle herders, that help them cope with unpredictable environments, innovation is less common in urban dwelling hyenas. The consequences of this reduction in innovative behavior are not clear, though innovative behavior can modulate fitness trade-offs, like increased reproductive success with decreased offspring survival, in spotted hyenas.
Ecology
Diet
The spotted hyena is the most carnivorous member of the Hyaenidae. Unlike its brown and striped cousins, the spotted hyena is primarily a predator; this has been shown since the 1960s. One of the earliest studies to demonstrate their hunting abilities was done by wildlife ecologist Hans Kruuk, and he showed through a 7-year study of hyena populations in the Serengeti and Ngorongoro Crater that spotted hyenas hunt as much as lions, with later studies showing this tendency in many other areas of Africa. There are however large differences between populations, depending on their habitat, available prey species and the presence of other predators. Thus the estimated contribution from hunting to their diet ranges from at least half up to 98%, the remainder being from scavenging. 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. Cape buffalo are rarely attacked due to differences in habitat preference, though adult bulls have been recorded to be taken on occasion. In Kruger National Park, blue wildebeest, cape buffalo, plains zebra, greater kudu and impala are the spotted hyena's most important prey, while giraffe, impala, wildebeest and zebra are its major food sources in the nearby Timbavati area. Springbok and kudu are the main prey in Namibia's Etosha National Park, and springbok in the Namib. In the southern Kalahari, gemsbok, common eland, lechwe, waterbuck, wildebeest and springbok are the principal prey. In Chobe, the spotted hyena's primary prey consists of migratory zebra and resident impala. In Kenya's Masai Mara, 80% of the spotted hyena's prey consists of topi and Thomson's gazelle, save for during the four-month period when zebra and wildebeest herds migrate to the area. Bushbuck, suni and buffalo are the dominant prey items in the Aberdare Mountains, while Grant's gazelle, gerenuk, sheep, goats and cattle are likely preyed upon in northern Kenya. Unlike other large African carnivores, spotted hyenas do not preferentially prey on any species, and only African buffalo and giraffe are significantly avoided. Spotted hyenas prefer prey with a body mass range of 56–182 kg (123–401 lb), with a mode of 102 kg (225 lb). 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 anti-predator behaviours. Small prey is killed by being shaken in the mouth, while large prey is eaten alive.
Enemies and competitors
Lions
Where spotted hyenas and lions occupy the same geographic area, 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%. Lions typically ignore spotted hyenas, unless they are on a kill or are being harassed by them. There exists a common misconception that hyenas steal kills from lions, but most often it is the other way around, and lions will readily steal the kills of spotted hyenas. In the Ngorongoro Crater, it is common for lions to subsist largely on kills stolen from hyenas. Lions are quick to follow the calls of hyenas feeding, a fact demonstrated by field experiments, during which lions repeatedly approached whenever the tape-recorded calls of hyenas feeding were played. 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 eating. In some cases, spotted hyenas are bold enough to feed alongside lions, and may occasionally force lions off a kill. This mostly occurs during the nighttime, when hyenas are bolder. Spotted hyenas usually prevail against groups of lionesses unaccompanied by males if they outnumber them 4:1. In some instances they were seen to have taken on and routed two pride males while outnumbering them 5:1. The two species may act aggressively toward one another even when there is no food at stake. Lions may charge at hyenas and maul them for no apparent reason; one male lion was filmed killing two hyenas on separate occasions without eating them, 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. 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.
Other felids Although cheetahs and leopards preferentially 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, while leopards, particularly males, may stand up to hyenas. The