Mary L. Weldele

A comparison of innovative problem-solving abilities between wild and captive spotted hyaenas, Crocuta crocuta

Innovative problem solving enables individuals to deal with novel social and ecological challenges. However, our understanding of the importance of innovation for animals in their natural habitat is limited because experimental investigations of innovation have historically focused on captive animals. To determine how captivity affects innovation, and whether captive studies of animal innovation suffer from low external validity, we need experimental investigations of innovation in both wild and captive populations of the same species in diverse taxa. Here we inquired whether wild and captive spotted hyaenas differ in their ability to solve the same novel technical problem, and in the diversity of exploratory behaviours they exhibit when first interacting with the problem. Our results suggest that wild and captive populations show important differences in their innovative problem-solving abilities. Captive hyaenas were significantly more successful at solving the novel problem, and significantly more diverse in their initial exploratory behaviour, than were wild hyaenas. We were able to rule out hypotheses suggesting that these differences result from excess energy or time available to captive animals. We conclude that captive hyaenas were more successful because captive individuals were less neophobic and more exploratory than their wild counterparts. These results have important implications for our interpretation of studies on innovative problem solving in captive animals and aid our attempts to gain a broader understanding of the importance of innovation for animals in their natural habitat.

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.

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.

Distribution of Vasopressin in the Forebrain of Spotted Hyenas

The extreme virilization of the female spotted hyena raises interesting questions with respect to sexual differentiation of the brain and behavior. Females are larger and more aggressive than adult, non‐natal males and dominate them in social encounters; their external genitalia also are highly masculinized. In many vertebrates, the arginine vasopressin (VP) innervation of the forebrain, particularly that of the lateral septum, is associated with social behaviors such as aggression and dominance. Here, we used immunohistochemistry to examine the distribution of VP cells and fibers in the forebrains of adult spotted hyenas. We find the expected densely staining VP immunoreactive (VP‐ir) neurons in the paraventricular and supraoptic nuclei, as well as an unusually extensive distribution of magnocelluar VP‐ir neurons in accessory regions. A small number of VP‐ir cell bodies are present in the suprachiasmatic nucleus and bed nucleus of the stria terminalis; however, there are extensive VP‐ir fiber networks in presumed projection areas of these nuclei, for example, the subparaventricular zone and lateral septum, respectively. No significant sex differences were detected in the density of VP‐ir fibers in any area examined. In the lateral septum, however, marked variability was observed. Intact females exhibited a dense fiber network, as did two of the four males examined; the two other males had almost no VP‐ir septal fibers. This contrasts with findings in many other vertebrate species, in which VP innervation of the lateral septum is consistently greater in males than in females. J. Comp. Neurol. 498:80–92, 2006.

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.

Ultrasonic measurements of second and third trimester fetuses to predict gestational age and date of parturition in captive and wild spotted hyenas Crocuta crocuta

Parturition in spotted hyenas (Crocuta crocuta) is a fascinating event to witness, as females of this species are highly masculinized and give birth through a penis-like clitoris. Furthermore, shortly after birth, a high rate of aggression occurs between littermates that can sometimes end in siblicide. To study these events thoroughly, an accurate estimate of the date of parturition is necessary. To this end, we performed transabdominal ultrasounds every 20-30 days in five captive spotted hyenas of known gestational age, beginning approximately 30 days after mating. We measured the femur length (FL), abdominal circumference (AC), and biparietal diameter (BPD) of eight fetuses from Days 42 to 100 of their 110 days of gestation. FL proved to be the most effective measurement, as it correlated well with gestational age and was easy to obtain consistently. The relationship between estimated gestational age (EGA) and FL is described by the equation: [EGA = 37.3 + (14.0 x FL)]. AC also correlated well with EGA, but was more difficult to measure than FL. Measuring BPD became increasingly difficult as pregnancies advanced beyond 70 days of gestation. Because gestational age is often not known in captive and free-ranging spotted hyenas, measuring fetal FL ultrasonographically is a rapid and reliable way to determine an approximate date of parturition. This technique proved invaluable when used to track and monitor a free-ranging spotted hyena during the days just before and after parturition.

Effects of Prenatal Treatment with Antiandrogens on Luteinizing Hormone Secretion and Sex Steroid Concentrations in Adult Spotted Hyenas, Crocuta crocuta

Abstract Prenatal androgen treatment can alter LH secretion in female offspring, often with adverse effects on ovulatory function. However, female spotted hyenas (Crocuta crocuta), renowned for their highly masculinized genitalia, are naturally exposed to high androgen levels in utero. To determine whether LH secretion in spotted hyenas is affected by prenatal androgens, we treated pregnant hyenas with antiandrogens (flutamide and finasteride). Later, adult offspring of the antiandrogen-treated (AA) mothers underwent a GnRH challenge to identify sex differences in the LH response and to assess the effects of prenatal antiandrogen treatment. We further considered the effects of blocking prenatal androgens on plasma sex steroid concentrations. To account for potential differences in the reproductive state of females, we suppressed endogenous hormone levels with a long-acting GnRH agonist (GnRHa) and then measured plasma androgens after an hCG challenge. Plasma concentrations of LH were sexually dimorphic in spotted hyenas, with females displaying higher levels than males. Prenatal antiandrogen treatment also significantly altered the LH response to GnRH. Plasma estradiol concentration was higher in AA-females, whereas testosterone and androstenedione levels tended to be lower. This trend toward lower androgen levels disappeared after GnRHa suppression and hCG challenge. In males, prenatal antiandrogen treatment had long-lasting effects on circulating androgens: AA-males had lower T levels than control males. The sex differences and effects of prenatal antiandrogens on LH secretion suggest that the anterior pituitary gland of the female spotted hyena is partially masculinized by the high androgen levels that normally occur during development, without adverse effects on ovulatory function.