Effects of dispersal status on pituitary and gonadal function in the male spotted hyena

Male spotted hyenas (Crocuta crocuta) reach puberty at 24 months of age and then usually emigrate from their natal clans one to 52 months later. Recent work has shown that reproductive success is very low among adult males still residing in their natal groups, and it is similarly low among recent or "short-term" immigrants. Long-term immigrants father the vast majority of cubs born. Here we inquired whether these differences in reproductive success might be associated with variation among males in pituitary or gonadal function. In one free-living hyena population in Kenya, we compared baseline levels of plasma luteinizing hormone (LH) and testosterone (T) among adult natal males, short-term immigrants, and long-term immigrants, and we also compared their pituitary and gonadal responses to GnRH challenge. Mean basal plasma LH values did not differ among groups, but mean basal T concentrations in long-term immigrants were higher than those in either natal males or short-term immigrants. Similarly, pituitary response to GnRH challenge did not vary significantly among groups, but testicular response to challenge was greater in long-term immigrants than in natal males or short-term immigrants. Thus adult natal and immigrant males exhibited similar pituitary function but testicular function was attenuated among adult males that had not yet left their natal groups and also among males attempting to become established in new social groups. This suggests that, like the act of emigration itself, the process of social integration during immigration may have important physiological consequences for male mammals transferring between groups.     

Male spotted hyenas (Crocuta crocuta) queue for status in social groups dominated by females

A long-term study of immigrant male spotted hyenas (Crocuta crocuta) living in large multimale/multifemale groups (clans) demonstrated that males acquire social status by queuing. Maximumlikelihood estimates of parameters of a stochastic queuingmodel that assessed queuing discipline confirmed that immigrantmales respected the convention that their positions in a queueof typically 15 or more individuals was determined by theirsequence of arrival. Levels of aggression among males were low;males did not attempt to improve their social status throughphysical contests. Size and body mass did not influence malesocial status. The stability of queues was insured by an increasein the rate at which males formed coalitions against othermales as they rose in social status and by coalitions between high-ranked males and dominant females. High-ranked, long-tenuredmales chiefly consorted with ("shadowed") and focused theiraffiliative behavior on females of high reproductive valueand disrupted attempts by subordinate males to associate withthese females. High-ranked males also supported females againstlower-ranked males that harassed them. In contrast, lower-ranked,short-tenured males focused their affiliative behavior on young adult females and rarely shadowed or defended females. Malesthat did not disperse from their natal clan (nondispersers)quickly acquired top rank in the male social hierarchy. Irrespectiveof the social status acquired from their mother when young,nondisperser adult males submitted to all adult females.     

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.     

Reproductive skew among males in a female-dominated mammalian society

The purpose of this study was to document patterns of reproductiveskew among male spotted hyenas (Crocuta crocuta), a speciesin which many normal mammalian sex roles are reversed. We usedpaternity determined from 12 microsatellite markers togetherwith demographic and behavioral data collected over 10 yearsfrom a free-living population to document relationships among reproductive success (RS), social rank, and dispersal statusof male hyenas. Our data suggest that dispersal status andlength of residence are the strongest determinants of RS. Natalmales comprise over 20% of the adult male population, yet theysire only 3% of cubs, whereas immigrants sire 97%. This reproductiveadvantage to immigrants accrues despite the fact that immigrants are socially subordinate to all adult natal males, and it providesa compelling ultimate explanation for primary dispersal inthis species. High-ranking immigrants do not monopolize reproduction,and tenure accounts for more of the variance in male reproductivesuccess than does social rank. Immigrant male hyenas rarelyfight among themselves, so combat between rivals may be a relativelyineffectual mode of sexual selection in this species. Instead,female choice of mates appears to play an important role in determining patterns of paternity in Crocuta. Our data supporta "limited control" model of reproductive skew in this species,in which female choice may play a more important role in limitingcontrol by dominant males than do power struggles among males.     

Hunting rates and hunting success in the spotted hyena (Crocuta crocuta)

Hunting group size, hunting rates and hunting success were monitored over a seven-year period among members of one large clan of spotted hyenas ( Crocuta crocuta ) inhabiting the Masai Mara National Reserve, in south-west Kenya. Prey availability varied seasonally in this study area, and hyenas tended to hunt whichever prey species were most abundant during each month of the year. Over 75% of 272 hunting attempts were made by lone hyenas, even when they hunted antelope three times their own body mass, such as wildebeest and topi. Of all prey that were commonly hunted, only zebra were usually hunted in groups. Approximately one-third of all hunting attempts resulted in prey capture. Although no significant sex differences were observed in juvenile or adult hunting rates, low-ranking adult females hunted at significantly higher hourly rates than did higher-ranking females. Hunting success was not influenced by the social rank of hunters, but hunting group size and hunter's age strongly influenced success. Young hyenas were poor hunters, and did not achieve adult competency levels until they were 5–6 years old.     

Fission of a Spotted Hyena Clan: Consequences of Prolonged Female Absenteeism and Causes of Female Emigration

We describe the fission of one large East African clan of spotted hyenas (Crocuta crocuta). During an 8-mo period from late 1989 to early 1990, 8 of 22 adult females vanished from the clan, along with their juvenile offspring. 6 of these 8 adult females formed a new clan in an area adjacent to the parent clan's home range. The 6 adult female dispersers belonged to three mid- or low-ranking matrilines in the parent clan. Two juvenile males returned to the parent clan for temporary visits, and three female members of one matriline rejoined the parent clan after absences of over 8 mo. Returning females, but not males, were targets of severe aggression by adult female residents of the parent clan, and by juvenile residents of both sexes. Returning females fell from their previous mid-ranking positions to the bottom of the adult female hierarchy. Our data suggest that clan fission was promoted by the simultaneous occurrence of low food availability, an unusually high density of higher-ranking conspecific competitors, and the availability of neighboring vacant habitat.     

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.     

扩散或不扩散：雄性太行山猕猴繁殖成功比较研究

典型的猕猴（Macaca multta）社群为多雄多雌型,雌性留群并形成母系单元,雄性多在亚成年或成年期离开出生群,而群内成年雄性多为外部迁入个体。雄性的迁出被认为可降低近亲繁殖或提升繁殖成功。然而,诸多野外数据显示,少数本群出生雄性个体会居留于出生群一年或数年。尽管驱动雄性离群的因素较复杂（如社会关系、近亲回避、繁殖成功）,但繁殖成功的差异可能是驱动雄性离群的主导因素。为探讨居留于出生群是否影响雄性的繁殖成功,于2010年3月至2014年1月,在太行山猕猴国家级自然保护区王屋山地区,以一群野生太行山猕猴为研究对象,采用非损伤取样法并结合分子生物学方法,分析了群内出生和迁入成年雄性个体的繁殖成功（以子代数量评估）。研究发现：(1)群内51只子代个体中有36只个体可以匹配到其遗传学父亲;(2)4个迁入雄性繁衍了34个子代,仅1只群内出生雄性ZM繁衍了2只子代,但群内出生的雄性BB未匹配到子代。本研究提示,迁入雄性较本群出生雄性的繁殖成功较高,即迁移有助于繁殖成功的提升。     

Social status does not predict corticosteroid levels in postdispersal male spotted hyenas

In social species with low rates of direct male competition levels of corticosteroids should not correlate with social status. Male spotted hyenas acquire social status by observing strict queuing conventions over many years, and thus levels of male-male aggression are low, and male social status and tenure are closely correlated. In this study, we investigated whether the low rate of direct male competition in spotted hyenas was reflected in fecal corticosteroid levels of adult males in the Serengeti National Park. Also, interactions with dominant females may influence corticosteroid levels of males, and it has been suggested recently that males with a long tenure (high rank) are more stressed by females than males with a short tenure (low rank). We tested whether there is a difference in the likelihood of being aggressively challenged by dominant females between long-tenured and short-tenured males. Short-tenured males were more likely to elicit an aggressive response by females than long-tenured males, but previous work suggests that they also interacted less frequently with females, thus avoiding putting themselves in a potentially stressful situation. Thus, as expected, the comparison of males in three different clans revealed no correlation between social status or tenure and fecal corticosteroid levels. However, males of the largest clan had the highest levels of fecal corticosteroids, possibly reflecting higher rates of social interactions in larger clans.     

The effect of prey abundance and foraging tactics on the population dynamics of a social, territorial carnivore, the spotted hyena

We used naturally occurring spatial and temporal changes in prey abundance to investigate whether the foraging behavior of a social, territorial carnivore, the spotted hyena ( Crocuta crocuta ), conformed to predictions derived from the ideal free distribution. We demonstrate that hyenas in the Ngorongoro Crater, Tanzania, redistributed themselves from less profitable to more profitable areas, even when this required them to undertake foraging trips to areas beyond their clan territory boundary, or required normally philopatric females to emigrate. As expected for a system with rank related access to food resources in the territory, females of low social status foraged more often outside their territory and were more likely to emigrate than dominant females. Probably because Crater hyenas regularly foraged outside their territories, there was no correlation between clan size and prey density within territories, suggesting that clan sizes may have exceeded the carrying capacity of territories. A substantial decline of the hyena population in the Crater from 385 adults in the mid 1960s to 117 in 1996 was most likely due to a substantial decline of their main prey. The decline in the hyena population was associated with a decline in the size of clans but not in the number of clans. The number of clans probably remained constant due to emigration by females from large clans into vacant areas or clans with no adult females, and because hyenas regularly fed in areas containing concentrations of prey beyond their territory boundary. Between 1996 and 2003 annual recruitment rates of Crater hyenas consistently exceeded annual mortality rates, resulting in an almost doubling of the adult population. This increase was most likely due to an increase in prey abundance, a relatively low level of predation on hyenas by lions ( Panthera leo ), and an absence of high levels of disease related mortality.     

Male endocrine responses to females: Effects of social cues in cynomolgus macaques

This study tested the hypothesis that the hormonal responses of male macaques to sexually receptive females are mediated by specific socioenvironmental cues. Twelve, socially living male Macaca fascicularis were exposed to two-ovariectomized, estrogen-primed females under pair test, peer group, and peer group without dominant male conditions. Preexposure to postexposure changes in serum cortisol levels and testosterone levels were examined in relation to male dominance rank, age, and conditions of access to stimulus females. The males displayed significantly lower cortisol increases and greater testosterone increases with females under peer group than pair test conditions. Dominant males displayed greater testosterone increases than subordinate males under peer group conditions. The testosterone levels of subordinate males were greatly enhanced by removing the dominant male from each group. Adult males displayed greater cortisol responsivity to changes in conditions of access to females than did subadult males. Subadult males displayed greater testosterone responsivity to removal of the dominant male from the group than did adult males. It is concluded that specific social cues can greatly influence the endocrine responses of males to receptive females, and further, that there may be optimal socioenvironmental parameters for eliciting testosterone increases in male primates.     

Male Social Behavior and Dominance Hierarchy in the Sulawesi Crested Black Macaque (Macaca nigra)

In a 6-week study of the social behavior of wild Sulawesi crested black macaques (Macaca nigra), we found a linear and transitive dominance hierarchy among the six adult males in one social group. Dominance rank, as determined by the direction of supplantations, correlated strongly with percentage of time near more than four neighbors, frequency of grooming received from adult females, and percentage of time with an adult female as nearest neighbor. These results suggest that high-ranking males are socially attractive. Adult females sexually solicited high-ranking males more often than low-ranking males, but frequency of copulation was not correlated with dominance rank. Frequency and intensity of aggression between males are strongly correlated with rank distance, but aggression toward females was greatest for mid-ranking males. Males of all rank displayed significantly more aggression toward sexually receptive females than toward females in other estrous states. These data indicate that male Sulawesi crested black macaques display a social organization similar to that reported for multimale groups in other macaque species rather than the egalitarian social organization described for female Sulawesi macaques.     

Behavioural structuring of relatedness in the spotted hyena (Crocuta crocuta) suggests direct fitness benefits of clan-level cooperation

Spotted hyenas (Crocuta crocuta) are gregarious carnivores that live in multigenerational social groups, called clans, containing one to several matrilines. Members of multiple matrilines within a clan cooperate during dangerous interactions with inter- and intraspecific competitors. The evolution of cooperation may be influenced by relatedness between individuals, which in turn is influenced by reproductive skew and mate choice, dispersal and territorial behaviours. Behavioural data exist for spotted hyenas, but corresponding data on patterns of relatedness are unavailable; this lack of data makes it difficult to assess the relative importance of selection pressures favouring cooperative behaviour within and among groups. Therefore we conducted a longitudinal analysis of relatedness within a single large clan of spotted hyenas, as well as a cross-sectional analysis of relatedness among hyenas from multiple clans. Within a clan, patterns of relatedness reflected known pedigree relationships, and relatedness was higher within than among matrilines, even across generations. Although mean within-matriline relatedness varied among matrilines, it did not decline with matriline rank. On average, clan members were not related closely, due to high levels of male-mediated gene flow among clans, and relatedness declined very slightly across clan borders. Low mean relatedness within clans suggests that spotted hyenas cooperate with unrelated clan-mates against close paternal kin in other clans. Our data also suggest that spotted hyenas must derive large net direct fitness benefits from group living and cooperation.     

Social influences on plasma testosterone levels in male talapoin monkeys

Three social groups of laboratory-housed talapoin monkeys (Miopithecus talapoin) consisting of four adult males and four or five adult females, were observed over a 4-year period. All females were ovariectomized and given estradiol implants at intervals to render them sexually attractive; except for two castrated males with testosterone implants, all males were intact. Sexual and aggressive interactions were recorded, and testosterone levels were measured in plasma taken from males twice weekly. In each group males formed a linear dominance order, defined in terms of the direction of aggression between animals. The hormonal responses of intact males were monitored with respect to the presence of attractive females, access to these females, and transfer from the social group to isolation. In all groups the behavioral and endocrine responses of males to these treatments were rank related. In some instances, rising in rank was associated with elevated testosterone and falling in rank with decreased testosterone; these hormonal changes were associated with changes in sexual and aggressive interactions. The effects of sexual and aggressive behavior on plasma testosterone titers are discussed.     

Adult male replacement inMacaca fascicularis of East Kalimantan,Indonesia

This report on wild-ranging crab-eating macaques in East Kalimantan, Indonesia, describes male replacements for the first time in this species. A replacement at the alpha rank by an immigrant adult male was seen in this multimale troop during each year of the 20-month field study. The data show considerable variation in the process and outcome of social change. Adult male immigrants contested the alpha rank, whereas subadult male immigrants did not. The first replacement took 2 days, whereas the second one took 1 month. In the first replacement four males and 10 other residents left the troop. In the second replacement one of the two adult males was successful in immigrating when he replaced the resident male of his alpha rank, but the deposed alpha male was not evicted from the troop. Existing models of the causes of replacement (such as high density or human disturbance) and of the causes of infanticide are not supported by these data. Infanticide by immigrating males was not observed despite the apparent presence of the postulated circumstances conducive to infanticide.     

Reproductive biology of captive male cottontop tamarin monkeys as a function of social environment

The cottontop tamarin, Saguinus oedipus oedipus, is a cooperatively breeding monkey in which mature male and female offspring serve as helpers to assist in rearing younger siblings. Generally, only one female per social group reproduces; breeding restriction is mediated in postpubertal female offspring through low and acyclic levels of reproductive hormones. We investigated (1) reproductive activity of postpubertal male offspring, and (2) whether aggression towards male offspring and a cortisol-mediated stress response might restrict breeding of male offspring in the natal group. We examined sexual behaviour, olfactory communication and urinary hormone levels (testosterone, dihydrotestosterone, luteinizing hormone, cortisol) of the subject males while we manipulated their social environment from housing in natal groups to pairing with a novel female, and after the production of their own offspring. Mounting and erection rates of the male subjects were as high in the natal group as when paired with a novel female. However, most mounts in the natal group were directed towards other males, and complete copulation sequences did not occur with natal-group females. Social environment had no significant effect on olfactory investigation of breeding females. Although hormone levels increased significantly after the subjects were removed from the natal group, the elevation was transient; the hormone levels of subjects in their natal groups did not differ from the levels shown by the same males when successfully producing their own offspring. Male offspring received more contact aggression in the natal group than when paired with the novel female. However, most of the aggression was received from siblings rather than the breeding pair, and levels of cortisol did not correspond with levels of aggression. Thus, at both a behavioural and endocrine level, mature male offspring in captive natal groups were potentially fertile, but sexual activity with natal-group females appeared to be behaviourally restricted and directed instead towards group males. In wild cottontop tamarin groups, this reproductive potential may allow male helpers flexibility to respond to breeding opportunities. Copyright 2001 The Association for the Study of Animal Behaviour.     

Effects of natal male alliances on aggression and power dynamics in rhesus macaques

In the wild, male rhesus macaques disperse at sexual maturity. In captivity, however, males cannot disperse from their natal groups. Thus, the presence of natal males in captive rhesus social groups is unnatural and has the potential to negatively influence group dynamics and stability. A primary difference between natal males and non-natal (immigrant) males is that natal males have the opportunity to form long-term alliances with their maternal kin as well as nonkin. We investigated the factors associated with natal males' kin alliances and the impact of these alliances on measures of natal male behavior, group dynamics, and group stability. We found that natal males more frequently formed alliances with maternal kin when they were from high-ranking matrilines, had more siblings, and were younger. More frequent kin alliances were associated with more frequent use of intense aggression, higher individual rank, and higher degree of integration within the male displacement network. Thus, it seems that natal males use their alliances to be more active and influential in the social group, which may affect group stability. It appears that juvenile natal males from high-ranking matrilines, in particular, have the largest impact on group stability. Younger natal males from high-ranking matrilines formed alliances with kin more frequently and used intense aggression more frequently than older or lower ranking males. Furthermore, groups with a higher proportion of juvenile males from high-ranking matrilines also had higher rates of wounding. We suggest that the presence of natal males in rhesus groups may act in opposition to group stability.     

Endocrine aspects of social instability in the olive baboon (Papio anubis)

The relationships among social status and the cortisol and testosterone stress-response were studied in the non-natal male members of a troop of olive baboons (Papio anubis) before and during a period of social instability. The unstable period was characterized by dominance interactions that were more frequent, more inconsistent, and produced less linear hierarchies than during the stable period. These changes occurred predominantly among the high-ranking males. Such males engaged in coalitions and consortship harassments at a higher rate during the unstable period than during the stable period. Finally, high-ranking males had the highest rates of involvement in and initiation of escalated fighting during the unstable period, in contrast with the stable period. A number of endocrine correlates of instability emerged. During the stable period, high-ranking males (by reproductive criteria) showed an endocrine profile different from that of subordinates. They had the lowest basal cortisol titers, the largest and fastest increases in cortisol titer during stress, and had elevated testosterone titers during stress. None of these attributes was found in high-ranking males during the unstable period. Males during the unstable period had elevated basal cortisol titers, suppressed cortisol responsiveness to stress, and no longer showed elevated testosterone titers during stress. When psychological advantages associated with social status in a stable social environment were lost, endocrine efficiency previously associated with social status was apparently also lost. Further, high-ranking males, who were most aggressive exclusively during the unstable period, had the highest absolute titers of testosterone exclusively during the unstable period. Thus, elevated testosterone and high levels of aggression were unrelated to social status during the period of social stability, but were traits associated with dominant individuals during the unstable period.     

Endocrine correlates of rank,reproduction, and female-directed aggression in male Japanese macaques (Macaca fuscata)

Fecal testosterone and cortisol levels in six wild male Japanese macaques (Macaca fuscata), three of high rank and three of low, were analyzed to investigate the hormonal correlates of rank, reproduction, and female-directed aggression. The study encompassed the 6-month mating season, from October 1999 to March 2000, during which time 251 fecal samples and approximately 550 h of behavioral data were collected. Dominant males were not found to differ from subordinate males in overall rates of aggressive or copulatory behavior. Likewise, testosterone excretion, which peaked in the early part of the mating season and declined gradually thereafter, did not differ significantly by rank. High-ranking males, however, were observed to excrete significantly higher levels of cortisol than low-ranking males, suggesting that dominance may carry costs. The two hormones were found to be inversely correlated in the two most dominant males, but independent in all others. Rate of noncontact aggression was significantly correlated with testosterone, while no significant relationships were observed between testosterone and contact aggression nor any aspect of copulatory behavior. These data further support the contention that social subordinance and stress are not inexorably linked, as well as suggest that elevated glucocorticoid concentrations in high-ranking males may reflect increased metabolic costs associated with dominant male reproductive strategy.     

Endocrine correlates of contrasting male mating strategies in the European badger (Meles meles)

In mammals, testosterone secretion is known to respond rapidly to changes in males' immediate social environment. However, such changes do not take testosterone levels below the baseline required to maintain spermatogenesis, and so do not usually affect males' fertility. In this paper, we show that individual males' patterns of testicular activity reflect their social roles in a group-living carnivore, the European badger ( Melcs metes ), leading to individual and population differences in the seasonal patterns of both testosterone secretion and, apparently, spermatogenesis. In one badger population, some males left their natal groups to become breeding males in neighbouring territories. These males had higher plasma testosterone levels, and appeared to sustain spermatogenesis for a longer period, than males which remained in their natal territories. In contrast, in a second (higher density) population, males rarely transferred away from their natal territories, and appeared not to defend access to groups of females. Instead, males made forays to mate with females in neighbouring territories. In this population males had a shorter period of testicular activity, and there were no differences in testicular activity between immigrant and natal males.