Female Hyenas Research Articles

INDIVIDUAL VARIATION IN SPACE USE BY FEMALE SPOTTED HYENAS

Large carnivores range more widely than many other terrestrial mammals, and this behavior tends to bring them into frequent conflict with humans. Within any carnivore population, individual variation in patterns of space use should be expected to make some animals more vulnerable than others to risks of mortality from humans and other sources. In this study, our goal was to document variation among individuals in space use by female spotted hyenas (Crocuta crocuta). We examined predictions of hypotheses suggesting that space use by female hyenas is affected by reproductive state, social rank, and local prey abundance. Home-range size, distance at which females were found from the current communal den, and distance at which they were found from the nearest territorial boundary all varied significantly with the 3 independent variables. Females with den-dwelling cubs had smaller home ranges, were found closer to the communal den, and were found farther from the territorial boundary than were females with no den-dwelling cubs. Neither social rank nor prey availability significantly influenced the space-use patterns of females with den-dwelling cubs. Among females with no den-dwelling cubs, high-ranking females had smaller home ranges, were closer to the communal den, and were farther from the territorial boundary than were low-ranking females. The females ranging most widely were low-ranking individuals with no den-dwelling cubs when they were observed during periods of prey scarcity.

Androgens and the Role of Female “Hyperaggressiveness” in Spotted Hyenas (Crocuta crocuta)

It has been suggested that female dominance in spotted hyenas evolved due to selection for “hyperaggressive” androgenized females. According to this view, virilized external genitalia of female hyenas developed as a byproduct of selection for “androgen-facilitated social dominance.” The evidence that female hyenas have higher androgen levels than males or other female mammals is inconclusive. We compared concentrations of testosterone (T), 5α-dihydrotestosterone (DHT), and androstenedione (AE) from a population in the Serengeti. Females had significantly lower T and DHT levels than predispersal and postdispersal males. AE levels did not significantly differ between females and postdispersal males, but were significantly lower in predispersal males. Our results, and those from studies that have demonstrated that male and female hyenas experience similar levels of maternal androgens during fetal development, provide little support for a theory of selection for female dominance and hyperaggressiveness through enhanced secretion of androgens. Our data are consistent with an alternative view that female virilization is a byproduct of selection for precocial aggressive cubs of both sexes. According to this view, high investment in lactation favored selection for accelerated fetal development, high neonatal aggression, and facultative siblicide.

Mechanisms of maternal rank ‘inheritance’ in the spotted hyaena, Crocuta crocuta

Maternal rank ‘inheritance’, the process by which juveniles attain positions in the dominance hierarchy adjacent to those of their mothers, occurs in both cercopithecine primates and spotted hyaenas. Maternal rank is acquired in primates through defensive maternal interventions, coalitionary support and unprovoked aggression (‘harassment’) directed by adult females towards offspring of lower-ranking individuals. Genetic heritability of rank-related traits plays a negligible role in primate rank acquisition. Because the social lives of Crocuta and cercopithecine primates share many common features, we examined whether the same mechanisms might operate in both taxa to promote maternal rank ‘inheritance’. We observed a large clan of free-living spotted hyaenas in Kenya to test predictions of four mechanistic hypotheses. Hyaena rank acquisition did not appear to be directly affected by genetic heritability. Unprovoked aggression from adult female hyaenas was not directed preferentially towards low-ranking cubs. However, high-ranking mothers intervened on behalf of their cubs more frequently and more effectively than low-ranking mothers. Maternal interventions and supportive coalitions appeared to reinforce aggression directed at ‘appropriate’ conspecific targets, whereas coalitionary aggression directed at cubs apparently functioned to extinguish their aggressive behaviour towards ‘inappropriate’ targets. Young hyaenas and primates thus appear to ‘inherit’ their mothers' ranks by strikingly similar mechanisms.

Personality dimensions in spotted hyenas (Crocuta crocuta).

Personality ratings of 34 spotted hyenas (Crocuta crocuta) were made by 4 observers who knew the animals well. Analyses suggest that (a) hyena personality traits were rated with generally high reliability; (b) 5 broad dimensions (Assertiveness, Excitability, Human-Directed Agreeableness, Sociability, and Curiosity) captured about 75% of the total variance; (c) this dimensional structure could not be explained in terms of dominance status, sex, age, or appearance; and (d) as expected, female hyenas were more assertive than male hyenas. Comparisons with previous research provide evidence for the cross-species generality of Excitability, Sociability, and especially Assertiveness. Discussion focuses on methodological issues in research on animal personality and on the potential contributions this research can make for understanding the biological and environmental bases of personality.

The exaptive excellence of spandrels as a term and prototype.

In 1979, Lewontin and I borrowed the architectural term "spandrel" (using the pendentives of San Marco in Venice as an example) to designate the class of forms and spaces that arise as necessary byproducts of another decision in design, and not as adaptations for direct utility in themselves. This proposal has generated a large literature featuring two critiques: (i) the terminological claim that the spandrels of San Marco are not true spandrels at all and (ii) the conceptual claim that they are adaptations and not byproducts. The features of the San Marco pendentives that we explicitly defined as spandrel-properties-their necessary number (four) and shape (roughly triangular)-are inevitable architectural byproducts, whatever the structural attributes of the pendentives themselves. The term spandrel may be extended from its particular architectural use for two-dimensional byproducts to the generality of "spaces left over," a definition that properly includes the San Marco pendentives. Evolutionary biology needs such an explicit term for features arising as byproducts, rather than adaptations, whatever their subsequent exaptive utility. The concept of biological spandrels-including the examples here given of masculinized genitalia in female hyenas, exaptive use of an umbilicus as a brooding chamber by snails, the shoulder hump of the giant Irish deer, and several key features of human mentality-anchors the critique of overreliance upon adaptive scenarios in evolutionary explanation. Causes of historical origin must always be separated from current utilities; their conflation has seriously hampered the evolutionary analysis of form in the history of life.

2328 Metabolic defects and development of obesity in BRS-3 deficient mice

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.

2329 Analysis of genes expressed in androgenized female rats by differential display

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.

Sex determination in spotted hyena ( [formula omitted][formula omitted]) by restriction fragment length polymorphism of amplified ZFX/ZFY loci

We describe a quick and efficient method of determining the sex of DNA samples in the hyena. By choosing primers from sequences that are conserved between the human and bovine ZFY and ZFX genes, we amplified a 448 bp fragment from 1 male and 2 female hyenas. Using comparative sequencing, single base pair polymorphisms between the amplified ZFY and ZFX were established. Restriction fragment length polymorphism (RFLP) analysis with PstI and TaqI confirmed the sequence data and yielded specific banding patterns between the 2 sexes in the hyena.

Hormonal correlates of 'masculinization' in female spotted hyaenas (Crocuta crocuta). 1. Infancy to sexual maturity.

This report is concerned with hormone concentrations accompanying sexual maturation in a highly 'masculinized' female mammal, the spotted hyaena, Crocuta crocuta. Plasma concentrations of testosterone, androstenedione and oestrogen were determined by radioimmunoassay in a longitudinal study of 12 female and eight male hyaenas 2.5-62.5 months old. Concentrations of testosterone were significantly higher in males than in females after 26.5 months of age, but earlier measurements did not differ between sexes. Mean testosterone concentrations in adult female hyaenas (0.4-0.5 ng ml-1) were similar to those in several other female mammals that do not display a 'masculine' profile, but mean concentrations of androstenedione (2.5-5.5 ng ml-1) in female hyaenas were significantly higher than in males (1.0-2.0 ng ml-1), at most ages. Oestrogen could not be detected (less than 0.03 ng ml-1) in females until about 14 months of age and then increased (to approximately 0.13 ng ml-1) between 18 and 30 months; oestrogen remained undetectable in males. This rise in oestrogen in females corresponded to nipple enlargement and to changes in the size and elasticity of the urogenital meatus, permitting copulation and parturition through the clitoris. Gonadectomy (two males and four females) at 4-7 months resulted in nondetectable concentrations of testosterone and oestrogen and a marked attenuation in androstenedione (to approximately 0.39 ng ml-1), indicating that the gonads are the major source of these three steroids. Gonadectomy also eliminated sex differences in weight, nipple development and elasticity of the urogenital meatus.

Sex differences in the play behavior of immature spotted hyenas, Crocuta crocuta

Social, locomotor, and object play were studied in a colony of five male and five female peer-reared spotted hyenas during 12 1-hr tests while the animals were 13–19 months of age. Animals were tested in both same-sex and mixed-sex groups and were stimulated to play by the introduction of fresh straw and sawdust bedding. Each test was videotaped and the frequency of each type of play was determined by a time sampling procedure. Females played more frequently than males, however, the category of play which was elevated depended upon the social context during testing. In same-sex tests the frequency of vigorous social play displayed by females markedly exceeded that by males, but no comparable sex difference appeared in mixed-sex tests. Females engaged in locomotor play more frequently than males in mixed-sex tests, but no comparable sex difference appeared in same-sex tests. No sex difference in object play was observed. Two male and two female hyenas were gonadectomized prior to the initiation of the present sequence of tests. The results suggest that gonadectomy during the prepubertal period does not affect the frequency of play behavior. However, the small sample sizes preclude any conclusive determination of the effects of these gonadectomies on play.

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.