Adolescent male chimpanzees (Pan troglodytes) form social bonds with their brothers and others during the transition to adulthood

Social relationships play an important role in animal behavior. Bonds with kin provide indirect fitness benefits, and those with nonkin may furnish direct benefits. Adult male chimpanzees (Pan troglodytes) exhibit social bonds with maternal brothers as well as unrelated adult males, facilitating cooperative behavior, but it is unclear when these bonds develop. Prior studies suggest that social bonds emerge during adolescence. Alternatively, bonds may develop during adulthood when male chimpanzees can gain fitness benefits through alliances used to compete for dominance status. To investigate these possibilities and to determine who formed bonds, we studied the social relationships of adolescent and young adult male chimpanzees (N = 18) at Ngogo in Kibale National Park, Uganda. Adolescent male chimpanzees displayed social bonds with other males, and they did so as often as did young adult males. Adolescent and young adult males frequently joined subgroups with old males. They spent time in proximity to and grooming with old males, although they also did so with their age peers. Controlling for age and age difference, males formed strong association and proximity relationships with their maternal brothers and grooming relationships with their fathers. Grooming bonds between chimpanzee fathers and their adolescent and young adult sons have not been documented before and are unexpected because female chimpanzees mate with multiple males. How fathers recognize their sons and vice versa remains unclear but may be due to familiarity created by relationships earlier in development.     

Association partners of young chimpanzees in the Mahale Mountains National Park,Tanzania

Association partners of young chimpanzees at the Mahale Mountains National Park were analyzed. Juvenile and adolescent chimpanzees associated frequently with their mothers, although mother-offspring association decreased as the offspring grew up. Males tended to leave their mothers and associate with adult males, while females remained frequently associating with their mothers in early adolescence. In late adolescence and young adulthood, males usually associated with adult males and cycling adult females. Females may transfer into neighboring unit-groups in this stage. Although an immigrant female tended to be alone when her estrous cycle stopped, she associated with many individuals, in particular with adult males, when she resumed cycling. Some orphans were observed to associate frequently with particular adults. The findings were discussed in relation to the unique characteristics of chimpanzee social system.     

Relationships Between Adult Male and Maturing Mountain Gorillas (Gorilla beringei beringei) Persist Across Developmental Stages and Social Upheaval

Across the animal kingdom, long‐term social relationships outside the context of reproductive pair bonds are rare. However, they have been demonstrated in some mammals including primates, cetaceans, and social carnivores. The ontogeny of such relationships is likely to depend on the benefits individuals can gain by cultivating them. Previous studies demonstrated that young mountain gorillas (Gorilla beringei beringei) have strong relationships with adult males, but little is known about the longevity of these bonds. Here, we examine the temporal stability of proximity relationships between coresident adult male and maturing gorillas in the habituated population monitored by the Dian Fossey Gorilla Fund International's Karisoke Research Center in Volcanoes National Park, Rwanda. We used spatial proximity data to assess the strength of relationships between adult males and juveniles, and tracked these relationships as the juveniles matured into subadults (3–4 yr later; n = 229 dyads) and then young adults (7 yr later; n = 42 dyads). The proximity relationships of juveniles of both sexes predicted their proximity relationships with adult males in both subadulthood and young adulthood. However some young adult males who had lost their top adult male proximity partner from juvenilehood developed new relationships with older males that had risen in the dominance hierarchy. These data suggest that (1) kin selection may play a more important role in social relationships between potential fathers and adult female offspring than previously suspected, and (2) when maturing males' foremost adult male social partners remain available to them, their relationships can be stable past the age at which younger males become reproductive competitors.     

Age differences in social interactions of young males in a chimpanzee unit-group at the Mahale Mountains National Park,Tanzania

The behavior and social interactions of young male chimpanzees were studied in relation to their age change. The data were obtained at the Mahale Mountains National Park, during a four-month period in 1986. Early adolescent males, becoming independent of their mothers, spend a long time near adults of both sexes. Late adolescent males are not tolerated by the senior males. Although such animals do not stop traveling together with their seniors, they are separated from the other members including the males of their own age class, and each of them lives a relatively lonely life. Where seniors are not nearby, they perform charging displays in front of estrous females. Young adult males tend to remain in the proximity of the alpha male, and can associate with their seniors without pant-grunting. Although some young adult males dominate over some senior males, increasingly performing charging displays, they do not appear to be permitted to associate intimately with their seniors; they are not yet considered to have attained social maturity. Prime and senior males are strongly bonded with one another, being able to associate intimately with those of their own or senior age classes including the alpha male. A young adult male's rise in rank is not connected with joining the “adult male-cluster,” nor does a senior male's decline necessarily means his dropping out from the cluster: the social position of male chimpanzees cannot be understood solely from their agonistic dominance rank. The alpha male plays a leading part in integrating the males of the unit-group. Young adult males and their seniors tend to associate most frequently with him, and all the males of the early adolescent or senior age classes pay attention to his movements.     

Sex Differential Behavior of Immature Hanuman Langurs (Presbytis entellus) in Ramnagar, South Nepal

We investigated sex differences in the social behavior of immature Hanuman langurs (Presbytis entellus) in the light of sex-specifically different life-courses and Hanuman langur characteristics, such as the individualistic dominance hierarchy and the rarity of intragroup coalitions among adult females. We observed four immature female and four immature male langurs—all members of the same free-ranging multimale multifemale group in Ramnagar, South Nepal—from November 1992 to February 1993 for 288 hr via focal-animal and instantaneous sampling techniques. Immature females spent significantly more time in proximity to other group members than immature males did. They had more physical contact and groomed more. Other immature females were their preferred social partners. Immature males also preferred like-aged females. They restricted their relationships with other immature males to proximity and occasional grooming. Monitoring was directed especially toward adult males. Female behavior can be interpreted as oriented toward integration into the female social network and their age-inverted dominance hierarchy. Males seem to prepare for leaving their natal group and for future strong intrasexual competition.     

Agonistic Interactions of Juvenile Savanna Baboons

19 juvenile members of known genealogies in two wild baboon groups were studied over a 16-month period to compare the ontogeny of agonistic experience and dominance relations for males and females. Juveniles of all age-sex classes were disproportionately likely to receive aggression from and submit to adult males per unit of time spent in proximity. This pattern intensified with increasing juvenile age. With age, juvenile females more often submitted to unrelated adult females from higher-ranking families, whereas this was not true for juvenile males. All juveniles received aggression from older group members more often during feeding than was expected by chance. High rates of agonistic interaction with unrelated adult females accounted for old juvenile females (3–5.5 years-old) interacting agonistically more frequently than male age peers and young juveniles of either sex (1–2.5 years-old). Adult females were also more aggressive toward females among young juveniles, suggesting that adult females target females among juveniles for aggression and resistance to rank reversal. Within juvenile age groups, males dominated all females and all younger males, irrespective of maternal dominance status. Dominance relations among female age-peers were generally isomorphic with relations among their mothers. No juvenile targeted any older male for rank reversal. Males targeted all older females, whereas females typically targeted only older females from families lower-ranking than their own. The strong sexual dimorphism in adult body size in baboons may explain why juvenile males' dominance relations with peers and adult females are not structured along lines of family membership as is true for the less dimorphic macaques. Acquisition of higher agonistic status probably allows juveniles of both sexes to increase their success in within-group feeding competition during late stages of juvenility, which, in turn, could affect important life-history traits such as age at menarche and adult body size.     

The role of male age, sperm age and mating history on fecundity and fertilization success in the hide beetle

Models of age-related mate choice predict female preference for older males as they have proven survival ability. However, these models rarely address differences in sperm age and male mating history when evaluating the potential benefits to females from older partners. We used a novel experimental design to assess simultaneously the relative importance of these three parameters in the hide beetle, Dermestes maculatus. In a two-part experiment we first explored age-related male mating success and subsequently examined the consequences of male age, sperm age and male mating history on female fecundity and fertilization success. In a competitive mating environment, intermediate-age males gained significantly higher mating success than younger or older males. To test the consequences for females of aged-related male mating success, a second set of females were mated to males varying in age (young, intermediate-age and old), in numbers of matings and in timing of the most recent mating. We found that male age had a significant impact on female fecundity and fertilization success. Females mated to intermediate-age males laid more eggs and attained consistently higher levels of fertilization success than females with young and old mates. A male's previous mating history determined his current reproductive effort; virgin males spent longer in copula than males with prior mating opportunities. However, differences in copulation duration did not translate into increased fecundity or fertilization success. There was also little evidence to suggest that fertilization success was dependent on the age of a male's sperm. The experiment highlights the potential direct benefits accrued by females through mating with particular aged males. Such benefits are largely ignored by traditional viability models of age-related male mating success.     

A comparison of the mating behavior of adolescent and adult female rhesus macaques (Macaca mulatta)

This study compares adult and adolescent female rhesus macaques with regard to (1) characteristics of their copulatory partners, (2) their proceptive behaviors, and (3) adult male behaviors toward them during estrus. We conducted focal follows of 24 adolescent and 65 adult free-ranging estrous female rhesus macaques on Cayo Santiago during two mating seasons. Compared to adult females, adolescents presented sexually to males at higher rates; copulated more frequently with rankless young male, and extra-group males; and, in one of two mating seasons, were ignored more frequently by males to whom they presented sexually. Adolescents tended to copulate with ranked, resident males at higher frequencies on days when the operational sex ratio (adult males:estrous adult females) was high. Males directed “muzzle-up” signals to adolescents at lower rates than to adults in one of two mating seasons, although this effect vanished when males who might have fathered adolescent females were excluded from analysis. Adolescents did not differ consistently from adults in strength of the correlation between proximity maintenance (dyadic Hinde's Index) and copulation rate, or in approach rate to males. Adolescent females, relative to adult females, presented sexually more to rankless young males, but did not present more to ranked, resident males. Both proximate (e.g. endocrine) and ultimate (e.g. differential fecundity; female-female mate competition) explanations may account for the reported differences between adult and adolescent female rhesus macaque sexuality.     

Which adult male savanna baboons form coalitions?

We investigated the mechanism of alliance formation among adult male savanna baboons by comparing the characteristics of males that formed coalitions frequently with males that never or seldom took part in coalitions. We observed three groups: two of Papio cynocephalus cynocephalusin Amboseli National Park, Kenya, and one of P. c. anubisin the vicinity of Gilgil, Kenya. We considered four hypotheses: (1) Males must be familiar with each other, (2) males must have an affinitive bond, (3) males must have more than average experience, and (4) the combined fighting ability of the coalition partners relative to the fighting ability of their opponent determines the likelihood that a coalition is formed. We conclude that relative fighting ability forms the key factor in coalition formation. High- ranking males do not form coalitions often, since they hardly need them. Low- ranking males rarefy form coalitions, since they cannot form effective coalitions among themselves. Affinity (“friendship”) may play a role as an additional factor. The relation of coalition formation with age and period of residence, which was found in several studies, can be explained largely by the correlation between these parameters and fighting ability.     

Changes in social interactions during adolescence in male mandrills (Mandrillus sphinx)

The adolescent period in male mandrills extends from the time the testicles descend (at the age of 3-4 years) to the time adult characteristics develop (at the age of 10 years), and is thus one of the longest adolescent periods in cercopithecines. In this short cross-sectional study of 11 male mandrills (4.7-9.1 years old), we analyzed social behavioral patterns to investigate partner preference and changes in types of interactions throughout puberty. The mandrills were separated into two clusters on the basis of all of the social interactions scored, as well as the age and sex of the protagonist. During early to mid puberty, immature individuals interacted preferentially with other male adolescents and juveniles. Playing was an important activity, and some affiliative interactions with juveniles were observed. Older adolescents interacted more with adult males and females. These older adolescents were predominantly aggressive toward other adolescents, females, and juveniles, and showed little or no affiliative or playful behaviors. These results indicate a shift in social partners: older males interacted more frequently with adult males, and their behavior involved more aggression and less submission compared to younger adolescents, which showed predominantly submissive and playful behavior. These changes are consistent with preparation for dispersal and future intermale competition.     

Social relationships and ritualized greetings in adult male baboons (Papio cynocephalus anubis)

Greetings involving exchanges of ritualized sexual gestures are a common form of interaction among adult male baboons, although relatively little attention has been paid to them. In this study, we investigate how greetings reflect important aspects of the male's social relationships, including dominance rank, age/residence status, and cooperative tendencies. The results are based on over 600 greetings among 12 adult males recorded during a 4-month study of a troop of wild olive baboons near Gilgil, Kenya. Four of the adult males were older, lower-ranking, long-term residents, which frequently formed coalitions to take estrous females away from the eight young, higher-ranking males. Virtually all dyads greeted: greetings occurred more than twice as often as other types of male-male interactions; and nearly all greetings occurred in a neutral context, in which there was no resource at stake. The percentage of greetings completed, the frequency with which different gestures were employed, and the roles adopted by each male varied significantly across old-old, old-young, and young-young dyads. Greetings between young adult males were often interrupted or actively resisted, consistent with their unstable and ambiguous dominance relationships. Greetings between old-old dyads were usually completed and appeared consistent with their cooperative relationships. One pair of old males formed a stable, reciprocal coalition against young males, and this pair's greetings showed remarkable symmetry of roles. Greetings, we hypothesize, function to allow males to negotiate important aspects of their relationships, including cooperation.     

Social interactions and the life history of femalePan paniscus in Wamba,Zaire

The unit-group of Pan paniscustends to form one large mixed party consisting of most of its members. Females usually stay in the party irrespective of their estrous state. They aggregate in the center of the party; and, older females stay in the most central part. Adult and adolescent sons of the old adult females stay in the central part more than males without mothers in the unit-group do. Females leave their natal unit-groups as older juveniles or in early adolescence and. settle in another unit-group after visiting several. Newly immigrated young females are eager to have social interactions with senior females to improve their social positions. Females become less eager to interact socially with other females when they have their own offspring. The strong bond between mother and son continues into his adulthood; and, females in old age become important members of the unit-group, both as the targets of association for younger females and as the mothers of highranking males. High social status of females seems related to their cohesive grouping tendency. The consistency of the multimale/multifemale party and the existence of prominent mother-offspring subunits are unique characteristics of P. paniscusamong the Pongidae. This social structure may provide a feasible model of the basic society from which human society evolved.     

The strategies of immature Macaques in their interactions with adult males in a colony ofMacaca fuscata

We investigated longterm socio-spatial relationships between adult males and immatures in a colony of Japanese macaques (Macaca fuscata fuscata), housed in a 1200 m² indoor-outdoor enclosure at Cavriglia Natural Park (Arezzo, Italy). Using focal animal observations together with scan sampling, we found that the immatures between six months and one year of age showed particularly high frequency of proximity and vicinity to the male troop leader. The immatures-actively sought proximity to this individual, even if social interaction with him was minimal compared to other males with which high frequency of play occurred. Proximity to the leader (even) caused some mild aggressive response by him, showing that this individual tolerated, rather than sought, proximity to the immatures. Their behaviour was not mediated by the mothers, who might be expected to profit from their offsprings’ proximity to the leader. The leader seemed to support the immatures during aggressive interactions with a significantly high frequency due to their spatial proximity to him. This behaviour decreased during the following year. We interpreted the immatures’ behaviour as a social strategy expressed during an early phase of individual ontogeny to manipulate the leader’s “control” role and to explore the physical and social environment from a relatively secure position.     

Sexual behavior of adult male chimpanzees of the Mahale Mountains national park,Tanzania

This study, based on 687 hr of focal observations, aims to describe overall patterns of the sexual behavior of the adult male chimpanzees of the Mahale Mountains, to compare the results with previous reports, and to explain the variations between studies. Genital inspection of cycling females by adult males was eight times as frequent as that of lactating females, and twice as frequent as that of pregnant females. Inspection of the genitals of cycling females increased dramatically 7–10 days before the onset of maximal swelling and gradually decreased as the day of ovulation approached. Adult males likely obtained information on the attractivity of females by inspecting their genitals. Mating was usually initiated by male courtship and followed by pelvic thrusts in a dorsoventral posture, performed on, rather than above, the ground, which continued for 7 s. on average, and was typically followed by female squeaking and darting from the male, or by the male grooming the female. Higher-ranking males mated with females in the peri-ovulatory period more frequently than did lower-ranking males. In particular, two alpha males mated with such females more often than did any other adult males. A male who interfered with a mating pair was dominant over the mating male in other agonistic contexts. The duration of intromission was correlated with neither dominance rank nor age. However, when an adult male declined in rank from alpha in 1991 to third in 1992, he showed a significantly shorter duration of intromission. This indicates that for a particular male, the alpha rank guaranteed longer duration of intromission. Allies of alpha males tended to mate with peri-ovulatory females more frequently than expected from their low dominance ranks. The number of mating partners was not correlated with male dominance rank, but was sometimes negatively correlated with male age. Females were significantly more likely to emit a copulatory squeak when mating with younger, rather than older, adult males. Male dominance rank and the rate of female copulatory squeaking were not correlated. Weaning infants regularly interfered with their mothers' mating. Occasionally, unrelated adolescent males and rarely females pushed themselves in between copulating adults. Female choice was indicated when they performed a “penis erection check” or took the initiative in courtship, or on the other hand showed strong reluctance to mate with particular males. Young adult males more often received erection checks than did prime males, while none of the three old adult males did. Courtship initiated by estrous females was not directed to two of the oldest males, the exception of which was the alpha male. The oldest males, except for the alpha, were consistently avoided by many estrous females, both young and old. In response to female reluctance, males behaved violently, however, this was not effective, because other more dominant males came to rescue the female. Neither courtship nor mating was seen between mature sons and their mothers, nor between brothers and sisters.     

Adaptive female choice for middle-aged mates in a lekking sandfly

Most theoretical models of age-related mate choice predict that females should prefer older males because they have proven survival ability. An alternative view is that older males represent inferior mates because of negative genetic correlations between early and late fitness components, or because older males have traded off longevity against other fitness components, have accumulated deleterious germ-line mutations, or are less well adapted to current conditions than more recently born individuals. While numerous studies have reported female choice for older males, few have explicitly examined the fitness consequences of such a preference. We present evidence from a lekking sandfly, Lutzomyia longipalpis, showing that choosy females discriminate against older males and gain a fitness benefit from their choice. When permitted free choice from an aggregation consisting of males aged zero to two days (young), four to six days (middle-aged) and eight to ten days (old), females preferentially mated with middle-aged males, but all measures of female reproductive success were independent of male age. In contrast, when a second set of females was randomly assigned single virgin males of known age, the eggs of those paired to old mates exhibited lower hatching success than the eggs of females mated to young or middle-aged males. These results suggest that females avoid mating with older males because they represent poorer quality mates. Age-related differences in male quality may have a genetic basis, but could equally well arise through a phenotypic decline in sperm quality or sperm transfer ability with male age. The lack of evidence of female discrimination against older males from other studies may be because these did not explore the reproductive success of the full age range of males.     

Proximal Spacing Between Individuals in a Group of Woolly Monkeys (Lagothrix lagotricha) in Tinigua National Park, Colombia

I studied proximal spacing within a group of woolly monkeys (Lagothrix lagotricha) during 7 months at Parque Nacional Tinigua, Colombia. I collected a total of 1188 instantaneous samples on focal individuals, recording the number and age/sex class of individuals that were in contact with, <2 m from, <5 m from the focal animal. The results indicate that proximate spacing reflects social affinities and is related to mother–infant relationship and social grooming. Subadult females and adult males are the sex/age classes with the lowest number of individuals in proximity. There are low proximity between adult females and between adult males and high frequencies of nearness between mother and offspring. Associations between males and females were usually low, but in some cases males showed preferences for a given female. There was a relatively gradual increase in spacing between mothers and their offspring as they became older. Old juvenile males were associated chiefly with other males—mostly subadults—whereas juvenile females maintained some proximity only to their mothers. There are also differences in spacing behavior according to different activity types.     

Long‐term proximity relationships in a captive social group of western lowland gorillas (Gorilla gorilla gorilla)

To visualize long‐term social relationships among 12 gorillas in a captive breeding group at the San Diego Wild Animal Park, San Diego, CA, the multidimensional scaling (MDS) procedure was applied to proximity (within 5 m) values collected in five different periods over 2.5 years. The resulting two‐dimensional representations clearly show that in samples taken during this 2.5‐year period, the silverback male was surrounded by five adult females, while three infant or young juvenile females, gathered in a body, remained between the silverback male and adult females. Some adult females maintained proximity to the silverback male more frequently than other adult females throughout the five periods. Unlike mountain gorillas in the wild, females with dependent offspring did not tend to stay near the silverback male more frequently than other females, and related females did not tend to spend more time near each other than non‐related females. Three older juvenile or young adult males were plotted the furthest from the silverback male, with gradual changes with increasing age. The usefulness of the MDS procedure, which can be used to visualize easily and clearly the social relationships among individuals, is discussed from the viewpoint of the management of breeding groups of captive gorillas. Zoo Biol 20:197–209, 2001. © 2001 Wiley‐Liss, Inc.     

Fate of ousted male residents of one-male bisexual troops of Hanuman langurs (Presbytis entellus) at Jodhpur,Rajasthan, India

Little is known about the fate of adult male residents after they are ousted from bisexual one-male troops of Hanuman langurs (Presbytis entellus) in the course of adult male replacements. In a long term study at Jodhpur, Rajasthan, it was possible to reconstruct partial life histories of several ousted residents. One resident was killed during the male change. Ousted residents did not regain residency despite their continued invasions into bisexual troops. It is assumed that the males' chances to take over and to defend a troop are restricted to an age of 9–14 years, when the males are in prime physical condition. One male became solitary for some months while trying to regain residency of his old troop, before joining some “alien” males. As a rule, males are likely to rejoin their own male bands if they are ousted after short periods of residency. If the residency exceeds 3 months then the ongoing structural change in the former band may prevent their reintegration. However, in such cases, ousted residents which belonged to the same band may reunite and mingle with another male band which lacks prime males. Weaned sons may follow their fathers after ousting. In the case of numerous weaned offspring, fathers and sons may together form at least temporary new male bands.     

A case report of a male rank reversal in a group of wild white-faced capuchins (Cebus capucinus)

During the course of a study of social relationships in wild, white-faced capuchins at Lomas Barbudal, Costa Rice (May 1990–May 1993), the alpha male was deposed by a subordinate male. The rank reversal was preceded by a decline in proximity maintenance by females to the alpha male, and an increase, in the amount of aggression directed toward the alpha male by the beta female and her female coalition partners. At the time of the rank reversal, females switched from giving thegargle vocalization exclusively to the old alpha male to gargling to the new alpha male; however, juveniles were less consistent with regard to which male they gargled to. At the time of the rank reversal, most adult females reduced the time spent in proximity and grooming with the old alpha male, and increased the time spent in proximity and grooming with the new alpha male. In contrast, juveniles' patterns of affiliation with males did not change in a predictable way following the reversal. The social strategies employed by capuchin monkeys during this rank reversal are compared with those of chimpanzees.     

Social influences on first reproductive success and related behaviors in the saddle-back tamarin (Saguinus fuscicollis,callitrichidae)

Some aspects of sociosexual behavior and the age at which maturing females experienced their first evident pregnancy and at which maturing males caused their first evident pregnancy were recorded in Saguinus fuscicolliscohabiting from 6 months of age with either an adult or a maturing sex partner. The following pair combinations and trios were studied: young male -young female, young male-adult female, adult male-young female, and adult male-young male-young female. The most frequent type of social interaction between young animals was rough and tumble play, while huddling was the most frequent interaction between young animals and their adult partners. Grooming and sexual interactions were very infrequent and there were no differences in the frequencies of these interactions among subject groups. Maturing females cohabiting with an adult male conceived significantly earlier than maturing females cohabiting with a male of their own age. Maturing males cohabiting with adult females sired offspring at a significantly earlier age than males cohabiting with a female of their own age. Some possible behavioral and physiological processes involved in the causation of early reproductive success in young tamarins cohabiting with adults are discussed. Saguinus fuscicollis fuscicollis andSaguinus fuscicollis illigeri.