Role-Reversed Nepotism Among Cubs and Sires in the Spotted Hyena (Crocuta crocuta)

Nepotism is widespread among parents and offspring, and is typically associated with fundamental asymmetries; parents can usually do more to help their offspring than vice versa, and the cost of a given nepotistic behavior is usually less for parents than for offspring. This may not be so among spotted hyenas (Crocuta crocuta); sires never achieve social rank equal to that of their cubs, to whom they provide no obvious paternal care. Nepotism by sires towards their cubs is thus socially constrained. However, the higher social status of cubs might offset cubs’ developmental disadvantages and permit nepotistic treatment of sires by offspring. We therefore sought to determine whether the interactions among spotted hyena cubs and adult males were influenced by kinship, using long‐term observations from one clan of spotted hyenas. Sires exhibited no overt nepotism towards their cubs in most behaviors, but they did associate more closely with their daughters than with unrelated control females. Sires also associated more closely with their daughters than with their sons, with whom they associated no more closely than they did with unrelated control males. Cubs favored their sires by directing less intense aggression towards them than towards unrelated control males. Cubs of both sexes also associated more closely with their sires than with control males after the cubs were independent of the clan's communal den. Although sires evidently recognize their offspring, paternal nepotism by sires towards their cubs is weaker than filial nepotism by cubs towards their sires. The small size and immaturity of cubs thus appear to be weaker constraints on nepotism than is the low social status of their sires.     

Sex Differences in Territorial Behavior Exhibited by the Spotted Hyena (Hyaenidae, Crocuta crocuta)

Spotted hyenas ( Crocuta crocuta ) are gregarious carnivores that defend group territories against encroachment by neighboring conspecifics. Here we monitored the behavior of members of one clan of free-ranging spotted hyenas during border patrols, 'wars' with neighboring clans, and other interactions with alien intruders, to document differences between the sexes in territorial behavior in this species. We also examined the possibility that the probability or rate of attack on alien hyenas encountered within the clan's territory would vary with the sex of the intruders. Initiation and leadership of most cooperative territorial behaviors were by adult female clan members, although border patrols were occasionally conducted by groups composed exclusively of resident males. The vast majority of alien intruders into the territory of the study clan were males. Resident females were more likely to attack intruding females than intruding males, but hourly rates of aggression directed by females towards aliens did not vary with intruder sex. Resident males were more likely than resident females to attack alien males, and resident males directed significantly higher hourly rates of aggression towards intruding males than females. Although female leadership in most cooperative territorial behaviors distinguishes spotted hyenas from many mammalian carnivores, other sex differences in the territorial behavior of spotted hyenas resemble those documented in other gregarious predators. Sex differences observed in hyena territoriality are consistent with the hypothesis that male and female clan members derive different selective benefits from advertisement and defense of group territories.     

Long-Read Genome Sequencing Provides Molecular Insights into Scavenging and Societal Complexity in Spotted Hyena Crocuta crocuta

The spotted hyena (Crocuta crocuta) is a large and unique terrestrial carnivore. It is a particularly fascinating species due to its distinct phenotypic traits, especially its complex social structure and scavenging lifestyle, with associated high dietary exposure to microbial pathogens. However, the underlying molecular mechanisms related to these phenotypes remain elusive. Here, we sequenced and assembled a high-quality long-read genome of the spotted hyena, with a contig N50 length of ∼13.75 Mb. Based on comparative genomics, immunoglobulin family members (e.g., IGKV4-1) showed significant adaptive duplications in the spotted hyena and striped hyena. Furthermore, immune-related genes (e.g., CD8A, LAG3, and TLR3) experienced species-specific positive selection in the spotted hyena lineage. These results suggest that immune tolerance between the spotted hyena and closely related striped hyena has undergone adaptive divergence to cope with prolonged dietary exposure to microbial pathogens from scavenging. Furthermore, we provided the potential genetic insights underlying social complexity, hinting at social behavior and cognition. Specifically, the RECNE-associated genes (e.g., UGP2 and ACTR2) in the spotted hyena genome are involved in regulation of social communication. Taken together, our genomic analyses provide molecular insights into the scavenging lifestyle and societal complexity of spotted hyenas.     

Endocrine aspects of sexual mimicry in Spotted hyaenas Crocuta crocuta

Female Spotted hyaenas mimic the male in the possession of a peniform and highly erectile clitoris and false scrotum. Sex hormones have been assayed in the blood plasma, gonads and adrenal glands of male and female Spotted hyaenas and in the blood plasma of Striped and Brown hyaenas. Although the testicular concentration of testosterone greatly exceeds that of the ovaries in Spotted hyaenas, there is no significant difference between the sexes in the mean plasma levels of this hormone, or of the other androgen assayed, andro-stenedione. In contrast, male Brown and Striped hyaenas have far higher plasma concentrations of testosterone than females.
Testosterone levels in twin female Spotted hyaena foetuses were similar to the mean for adult females and it is suggested that high foetal androgen levels are responsible for the appearance of the male sexual facies in adult female Spotted hyaenas. The high plasma androgen levels recorded in adult females may also be associated with their aggression and dominance of males.     

Territorial Behaviour by a Clan of Spotted Hyaenas Crocuta crocuta

Territorial behaviour of a clan of spotted hyaenas, Crocuta crocuta, was investigated in the Kruger National Park over a period of 27 months. These hyaenas were highly territorial, spending ? of their total activities on territory patrol by scent-marking intensively and monitoring 64 marking posts, particularly in border regions. Females, the more philopatric sex, were most active in territory defence. Local intensity of territorial activities by residents within their 130-km² territory was directly proportional to intrusion pressure by neighbours. When clan size was reduced, the ability to defend disputed land declined and larger neighbouring clans appropriated parts of the territory. We propose a relationship between resource distribution, intrusion pressure and territory defence.     

Measuring Faecal Epi-Androsterone as an Indicator of Gonadal Activity in Spotted Hyenas (Crocuta crocuta)

Enzyme immunoassays (EIA) that measure faecal testosterone metabolites (fTM) are useful tools to monitor gonadal activity. The aim of this study was to validate an “in-house” epiandrosterone EIA to monitor fTM in spotted hyenas. FTM were characterised in a male and a female hyena that each received an injection of ³H-testosterone. High-performance liquid chromatography (HPLC) analyses revealed a cluster of highly polar enzyme-hydrolysable hormone metabolite conjugates. We performed hydrolysis using β-glucuronidase to deconjugate metabolites and improve sensitivity of the assay. Because β-glucuronidase from Helix pomatia has been reported to bias testosterone measurements in some species, we compared the enzymatic activity of the commonly used β-glucuronidase extracted from H. pomatia with the same enzyme from Escherichia coli. Our results showed that β-glucuronidases from both sources produced similar results from spotted hyena faeces. We therefore hydrolysed samples with H. pomatia enzymes. HPLC analyses also demonstrated that following hydrolysis the epiandrosterone EIA measured significant amounts of immunoreactive metabolites corresponding to radiolabelled metabolites in both sexes. Additionally, HPLC and GC-MS analyses confirmed the presence of epiandrosterone in faeces of spotted hyenas. The biological relevance of the epiandrosterone EIA was validated by demonstrating (1) a significant increase in fTM levels in response to a testosterone injection within 16 h, (2) no biological responsiveness to an adrenocorticotropic hormone (ACTH) injection and (3) significant differences in fTM levels between juvenile males and adult immigrant males in a free-ranging wild population. Our results clearly demonstrate that the epiandrosterone EIA is a reliable non-invasive method to monitor gonadal activity in spotted hyenas.     

Androgen levels in the Spotted hyaena Crocuta crocuta: the influence of social factors

The Spotted hyaena is characterized by a suite of unique morphological and behavioural adaptations in the female: the external genitalia are nearly indistinguishable from those of the male, and females dominate males in most behavioural interactions. In a previous study of southern African hyaenas, males and females were found to have similar levels of circulating androgen, and it was suggested that relatively high foetal and adult levels are associated with female genital masculinization and dominance over males, respectively. This study shows that females from an East African population have androgen levels significantly lower than males, and that these levels in both sexes are strongly affected by individual social status; alpha animals had the highest androgen levels in each sex. These data cast doubt on the earlier hypothesis that aspects of sexual monomorphism in the Spotted hyaena are related solely to elevated female androgen titres.     

Spotted hyena (Crocuta crocuta) coexisting at high density with people in Wukro district,northern Ethiopia

We surveyed density and abundance of spotted hyena (Crocuta crocuta) in the highly degraded and prey depleted Wukro district, northern Ethiopia, with a human population density of 98 persons per square kilometer. A total of 117 spotted hyenas responded to callups, giving a hyena density of 52 hyenas per 100 km² or a total population of 535 hyenas in the district. We quantified the economic impact of spotted hyena predation on livestock using semi structured interviews with randomly selected households. Respondents indicated a total loss of 203 domestic animals to hyena depredation over the past five years. Average annual depredation per household was 0.13 livestock worth US$ 6.1. The diet of spotted hyenas was assessed in three sub-districts by scat analysis and showed 99% prey items of domestic origin, only three of 211 scat contained hair of Ethiopian hare (Lepus fagani) and porcupine (Hystrix cristata). We conclude that hyenas in northern Ethiopia live at high density and eat almost exclusively anthropogenic food and are not dependent on conservation areas.     

Social intelligence in the spotted hyena (Crocuta crocuta)

If the large brains and great intelligence characteristic of primates were favoured by selection pressures associated with life in complex societies, then cognitive abilities and nervous systems with primate-like attributes should have evolved convergently in non-primate mammals living in large, elaborate societies in which social dexterity enhances individual fitness. The societies of spotted hyenas are remarkably like those of cercopithecine primates with respect to size, structure and patterns of competition and cooperation. These similarities set an ideal stage for comparative analysis of social intelligence and nervous system organization. As in cercopithecine primates, spotted hyenas use multiple sensory modalities to recognize their kin and other conspecifics as individuals, they recognize third-party kin and rank relationships among their clan mates, and they use this knowledge adaptively during social decision making. However, hyenas appear to rely more intensively than primates on social facilitation and simple rules of thumb in social decision making. No evidence to date suggests that hyenas are capable of true imitation. Finally, it appears that the gross anatomy of the brain in spotted hyenas might resemble that in primates with respect to expansion of frontal cortex, presumed to be involved in the mediation of social behaviour.     

Sex-specific androgen binding in spotted hyaena (Crocuta crocuta) plasma

• 1.1. A charcoal adsorption assay demonstrated a large variance in androgen binding ability in female spotted hyaenas.
• 2.2. A positive correlation between plasma androgen binding ability and ovarian steroid concentrations was demonstrated in adult females.
• 3.3. The strong plasma binding affinity for testosterone and dihydrotestosterone (DHT) (nM) together with the lack of cortisol and weaker oestradiol-17β binding suggests that a specific androgen binding substance, possibly a protein, is present in adult females of this species.
• 4.4. The lack of high affinity binding in male spotted hyaenas is unusual and deserves further investigation.
• 5.5. Some androgen binding in all, including males and immature animals suggests that albumin may bind some plasma androgens in this species.

     

Masculinized otoacoustic emissions in female spotted hyenas (Crocuta crocuta)

In humans and rhesus monkeys, click-evoked otoacoustic emissions (CEOAEs) are stronger in females than in males, and there is considerable circumstantial evidence that this sex difference is attributable to the greater exposure to androgens prenatally in males. Because female spotted hyenas are highly androgenized beginning early in prenatal development, we expected an absence of sexual dimorphism in the CEOAEs of this species. The CEOAEs obtained from 9 male and 7 female spotted hyenas confirmed that expectation. The implication is that the marked androgenization to which female spotted hyenas are exposed masculinizes the cochlear mechanism responsible for CEOAEs. The CEOAEs measured in 3 male and 3 female hyenas that had been treated with anti-androgenic agents during prenatal development were stronger than the CEOAEs of the untreated animals, in accord with the implied inverse relationship between prenatal androgen exposure and the strength of the cochlear mechanisms producing CEOAEs. The CEOAEs of three ovariectomized females and two castrated males were essentially the same as those for the untreated females and males, suggesting that there is little or no activational effect of hormones on CEOAE strength in spotted hyenas. Distortion product OAEs (DPOAEs) also were measured. Those sex differences also were generally small (as they are in humans), and the effects of the anti-androgen agents were inconsistent. Thus, prenatal androgen exposure apparently does affect OAEs, but the effects appear to be greater for the reflection-based cochlear mechanism that underlies CEOAEs than for the nonlinear cochlear mechanism underlying DPOAEs.     

Spotted hyaena Crocuta crocuta feeding ecology and selectivity of large herbivorous prey in the Namib desert

We have investigated the relationship between spotted hyaenas in the south Namib Desert and large herbivorous prey and have summarized an updated overview of predator‐prey relationships in this resource‐limited arid environment. Over the 52‐month study, we recorded the densities (#/km⁻², ±SE) of the four local large herbivorous prey species: gemsbok (1.229, ±0.50), springbok (1.352, ±0.48), ostrich (0.648, ±0.23), and greater kudu (0.343, ±0.00). A fecal analysis was performed on 146 collected spotted hyaena scats, and prey items were identified and hairs cross‐follicle analyzed to the species level. Spotted hyaena diet at the study area remained opportunistic with 240 identified prey items representing eight differing prey species being recorded, ranging from ostrich eggs to large ungulates. The Ivlev''s Electivity Index was used to determine which large herbivorous prey was most selected for. Although gemsbok had a higher representation of prey items in the sampled scats, all sampled large herbivorous prey species scored below 0 and are thus generally avoided in relation to their availability in the environment. If any prey preferences are expressed by spotted hyaena in the Namib, it can be presumed to be a nonsampled prey species. We therefore promote further detailed investigations into all other prey species present, and seasonal variations of prey densities and scat sampling, within the study environment.     

Patterns of den occupation by the spotted hyaena (Crocuta crocuta)

Spotted hyaenas utilize isolated natal dens (NDs) and communal dens (CDs) for rearing their cubs. Here we describe patterns of natal and CD occupation by hyaenas belonging to one well‐studied clan in the Maasai Mara National Reserve during a 10‐year period. Locations of 98 den sites that were used as natal or CDs by hyaenas in the study clan were digitized in a Geographic Information System, and the duration of use of each den site, frequency of re‐use, and distances involved in den moves were quantified. Hyaenas moved their CD monthly on average. Most CD sites were occupied only once during the study, but several sites were used repeatedly. On rare occasions, the movement of hyaenas to a new den site could be attributed to a disturbance event at the CD, but factors regularly prompting hyaenas to move to new CD sites were unclear. High‐ranking female hyaenas were more likely to rear their cubs from birth in a CD than low‐ranking females. Low‐ranking females almost always utilized isolated NDs for the first few weeks of a litter's development, and low‐ranking females transferred their cubs over longer distances than did high‐ranking females.