Stephen E. Glickman

Competition and cooperation between litter-mates in the spotted hyaena, Crocuta crocuta

Abstract The development of intra-litter competition and cooperation is described in free-living and captive spotted hyaenas. Field data were collected on dominance relations in 26 twin litters, and additional behavioural analyses were performed on different subsets of this group. Intra-litter dominance relations were assessed on the basis of the direction of aggressive and appeasement behavior patterns. In all wild litters, one cub clearly dominated the other by the time cubs were observed above-ground, at 2–3 weeks of age. Within the 17 twin litters of mixed sex, female dominance over male litter-mates was significantly more common (N = 14) than the reverse (N = 3). When males were the dominant litter-mates, they were as aggressive towards their siblings as were females. Rates of intra-litter aggression were highest in the youngest age interval observed (1–2 months), and dropped significantly the next month. Peak monthly rates of intra-litter aggression correlated significantly with maternal rank, such that offspring of low-ranking females fought more than of those high-ranking females. High levels of intra-litter cooperation were observed in the context of coalition formation, and youngster affiliated more with litter-mates than with any other hyaena. In captivity, seven twin and two triplet litters were videotaped during the first 2 months of life, and were scored for aggressive interactions. Results showed that dominance between litter-mates is established as early in development as the first day of life.

Sexual dimorphism of perineal muscles and motoneurons in spotted hyenas.

Female spotted hyenas are known for their male‐like genitalia, high levels of aggression, and dominance over males, characteristics which are attributed to exposure to elevated levels of testosterone in utero. Although the nervous system of spotted hyenas has not previously been examined, one might predict that neural systems which are sexually dimorphic in other mammals would be monomorphic in this species. Spinal motoneurons which innervate muscles associated with the phallus are located in Onufs nucleus and are more numerous in males than in females in a wide array of mammals. Onufs nucleus was examined in adult and neonatal spotted hyenas and, contrary to expectation, was found to be sexually dimorphic in the typical mammalian pattern: Males have significantly more motoneurons in Onufs nucleus than do females. This dimorphism was correlated with a previously undescribed dimorphism in the relevant target musculature. Specifically, the morphology of the bulbocavernosus muscle is distinctly different in male and female spotted hyenas. Pregnant hyenas were treated with anti‐androgen in an attempt to interfere with the actions of androgen during fetal development. Motoneuron number in Onuf??s nucleus and the morphology of the bulbocavernosus muscle were feminized in males exposed to anti‐androgen in utero.

Effects of castration, blindness and anosmia on social reactivity in the male Mongolian gerbil (Meriones unguiculatus)

Abstract The effects of a varied set of hormonal and sensory variables were analyzed in terms of their impact upon social encounters between pairs of male gerbils. Control observations were employed to assess effects of these variables on behavior in the test situation when no other animal was present. Castration was found to increase aggression between male gerbils, without changing the basic patterns of solitary behavior. Removal of visual input (through blinding) resulted in some increment in aggressive interactions and marked facilitation of locomotor activity. Alternately, anosmia produced either through bilateral removal of the olfactory bulbs, or as the result of treatment of the peripheral mucosa with zinc sulphate, resulted in a general reduction in social interaction despite a moderate increment in locomotor activity.

Exposure to naturally circulating androgens during foetal life incurs direct reproductive costs in female spotted hyenas, but is prerequisite for male mating

Among all extant mammals, only the female spotted hyena (Crocuta crocuta) mates and gives birth through the tip of a peniform clitoris. Clitoral morphology is modulated by foetal exposure to endogenous, maternal androgens. First births through this organ are prolonged and remarkably difficult, often causing death in neonates. Additionally, mating poses a mechanical challenge for males, as they must reach an anterior position on the females abdomen and then achieve entry at the site of the retracted clitoris. Here, we report that interfering with the actions of androgens prenatally permanently modifies hyena urogenital anatomy, facilitating subsequent parturition in nulliparous females who, thereby, produce live cubs. By contrast, comparable, permanent anatomical changes in males probably preclude reproduction, as exposure to prenatal anti–androgens produces a penis that is too short and has the wrong shape necessary for insertion during copulation. These data demonstrate that the reproductive costs of clitoral delivery result from exposure of the female foetus to naturally circulating androgens. Moreover, the same androgens that render an extremely unusual and laborious process even more reproductively costly in the female are apparently essential to the males physical ability to reproduce with a normally masculinized female.

What the hyena's laugh tells: Sex, age, dominance and individual signature in the giggling call of Crocuta crocuta

BackgroundAmong mammals living in social groups, individuals form communication networks where they signal their identity and social status, facilitating social interaction. In spite of its importance for understanding of mammalian societies, the coding of individual-related information in the vocal signals of non-primate mammals has been relatively neglected. The present study focuses on the spotted hyena Crocuta crocuta, a social carnivore known for its complex female-dominated society. We investigate if and how the well-known hyenas laugh, also known as the giggle call, encodes information about the emitter.ResultsBy analyzing acoustic structure in both temporal and frequency domains, we show that the hyenas laugh can encode information about age, individual identity and dominant/subordinate status, providing cues to receivers that could enable assessment of the social position of an emitting individual.ConclusionsThe range of messages encoded in the hyenas laugh is likely to play a role during social interactions. This call, together with other vocalizations and other sensory channels, should ensure an array of communication signals that support the complex social system of the spotted hyena. Experimental studies are now needed to decipher precisely the communication network of this species.

Social Facilitation, Affiliation, and Dominance in the Social Life of Spotted Hyenasa

Spotted hyenas (Crocuta crocuta) are social carnivores, living in multifemale, multimale ‘‘clans.’ ’ ‘ s 2 With female philopatry and male dispersal, separate female and male dominance hierarchies, and female matrilines that constitute the fundamental social core of the clan, the social organization of spotted hyenas approximates that of many common old world monkeys in the broad outline of their ~ociali ty.~.~ Membership in the clan enables hyenas to hunt prey as large as zebra and is essential to defense of kills against lions and of hunting territories against other groups of hyenas. Spotted hyenas also display some rather unique characteristics. Adult females and their juvenile, or subadult, offspring dominate adult immigrant males in virtually all social interactions.“ In addition, hyenas often spend their days alone at solitary dens, typically reassembling in the late afternoon and socializing at the communal den before forming smaller hunting parties. For many hyenas there is a daily transition from a solitary existence to the intense, highly differentiated social interactions of life within the clan.’ All social carnivores display a delicate balance between cooperation and competition. In spotted hyenas, competition may simply be evinced by speed-of-eating at a kill. That is, with a group of hyenas feeding at a dead wildebeest and reducing it to a small pile of horns and hooves in less than 30 minutes, the individual that can eat most rapidly will have an advantage over colleagues that eat more slowly. Overt aggression and the formation of dominance hierarchies also play a role in access to resources, and dominance rank is directly related to ultimate reproductive success? The present paper focuses on the integration of cooperation and competition, and correlated behavioral mechanisms of aggression, dominance, and affiliation, within the social life of the spotted hyena. Towards that end, we focus on three themes that have emerged from our studies of these animals: (1) the emergence of individually differentiated systems underlying cooperation and competition from a more general tendency of hyenas to do-what-other-hyenas-are-doing; (2) the role of ‘ ‘meeting

The Ontogeny of the Urogenital System of the Spotted Hyena (Crocuta crocuta Erxleben)

Abstract Studies were conducted to elucidate the importance of androgen-mediated induction of the extreme masculinization of the external genitalia in female spotted hyenas. Phallic size and shape; androgen receptor (AR) and α-actin expression; and sex-specific differences in phallic retractor musculature, erectile tissue, tunica albuginea, and urethra/urogenital sinus were examined in male and female fetuses from Day 30 of gestation to term. Similar outcomes were assessed in fetuses from dams treated with an AR blocker and a 5α-reductase inhibitor (antiandrogen treatment). Clitoral and penile development were already advanced at Day 30 of gestation and grossly indistinguishable between male and female fetuses throughout pregnancy. Sex-specific differences in internal phallic organization were evident at Gestational Day 45, coincident with AR expression and testicular differentiation. Antiandrogen treatment inhibited prostatic development in males and effectively feminized internal penile anatomy. We conclude that gross masculinization of phallic size and shape of male and female fetuses is androgen-independent, but that sexual dimorphism of internal phallic structure is dependent on fetal testicular androgens acting via AR in the relevant cells/tissues. Androgens secreted by the maternal ovaries and metabolized by the placenta do not appear to be involved in gross masculinization or in most of the sex differences in internal phallic structure.

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.

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.

Responses to olfactory stimuli in spotted hyenas (Crocuta crocuta): I. Investigation of environmental odors and the function of rolling.

Olfaction is crucial to spotted hyenas (Crocuta crocuta), yet there are no controlled studies of their reactions to odors. In Experiment 1, the authors examined responses of captive hyenas to various environmental (prey, nonprey animal, and plant) odors. Subjects approached and sniffed all odors equally but preferentially licked prey odors, scent marked next to odors, and rolled in animal-based odors. In Experiment 2, the authors examined the function of rolling by applying odors to the pelts of captive hyenas. When hyenas wore carrion, they gained positive social attention (increased investigation and allogrooming) from pen mates, but when they wore camphor, the normal social greeting ceremony was curtailed. Thus, olfactory stimuli elicit specific responses, influence where behavior is directed, and can be used to affect social interaction.