Rank relations among sisters in semi-free-ranging Barbary macaques (Macaca sylvanus)

Although semi-free-ranging Barbary macaque females are able to outrank older females from lower-ranking matrilines (matrilineal rank acquisition), they do not systematically outrank their older sisters, as is known to be the case for semi-free-ranging rhesus monkeys (Macaca mulatta) and Japanese macaques (Macaca fuscata). We test the hypothesis that differences in the support received by younger sisters against their older sisters and against older lower-ranking females might account for this interspecific difference. Thirty-one sister dyads, members of a group of 109 Barbary macaques living at La Montagne des Singes, France, were observed during 16 months. The results indicate that (1) all females were dominant to their younger sisters, and the latter were never observed to challenge their older sisters; (2) younger sisters received as much kin support against their older sisters as against older lower-ranking females; (3) only very young females received support from their kin against their older sisters; (4) younger sisters received much more support from nonkin females against lower-ranking females than against their older sisters; and (5) Barbary macaque females appear to be supported against their older sisters less frequently than rhesus macaque females are. We conclude that the lack of nonkin support is the main factor accounting for the failure of younger sisters to outrank their older sisters in Barbary macaques. Initially this might result from kin support not being sufficient to induce younger sisters to challenge and to solicit support against their older sisters.     

Coalition formation among male Barbary macaques (Macaca sylvanus)

A coalition is formed when one animal intervenes in an ongoing conflict between two parties to support one side. Since support of one party is also an act against the other party, coalitions are triadic interactions involving a supporter, a recipient, and a target. The purpose of this study was to test which of three possible theories explains coalition formation among male Barbary macaques: 1) Males support kin to enhance their indirect fitness (kin selection). 2) Males support nonkin to receive future reciprocal support (reciprocal altruism). 3) Males pursue self-interests and immediately benefit via nonkin support (cooperation). Coalition formation was investigated among 31 semi-free male Barbary macaques in the Salem Monkey Park, Germany during the mating season. The results show: 1) Males intervened more often in dyadic conflicts in which a related opponent was involved and supported related opponents more than unrelated opponents. Close kin supported each other more often than distant kin. 2) Some evidence for reciprocal support was found. However, reciprocity was probably a by-product of targeting the same individuals for dominance. 3) Coalition formation among nonkin is best interpreted as cooperation, based on self-interests. Male Barbary macaques seem to intervene more often to stabilize and less often to improve their rank. Although our data were limited, the results revealed that kin support, reciprocal support, and cooperative support were all involved in coalition formation among male Barbary macaques.     

Juveniles Outrank Higher-Born Females in Groups of Long-Tailed Macaques with Minimal Kinship

In a typical matrilineal or nepotistic hierarchy a mother's rank sets both her daughter's lowest rank (above lower-born females), and her daughter's highest rank (below the mother and higher-born females). Long-tailed macaques (Macaca fascicularis) form typical matrilineal dominance orders. We report a variant of this system that we observed in 4 groups of captive long-tailed macaques characterized by an unusual kinship structure. Each group was composed of the smallest possible matrilineages (mother-offspring pairs), the mothers being unrelated to each other. In each group, juveniles ranked above all the females subordinate to their mother, as this is the case in a typical matrilineal hierarchy, but a majority of juveniles of both sexes outranked their own mothers and/or several higher-born females and their offspring. Adult females resisted the juveniles and were 2.5 times heavier than the latter. The patterning of interventions in conflicts suggests that this unusual ranking pattern resulted from the existence of bridging alliances between the juveniles and individuals ranking above the juveniles' targets. The results indicate that the sole presence of the mother is sufficient for a daughter to outrank the females subordinate to her mother, but it is not sufficient to prevent the daughter from ascending the rank order. Our data suggest that in the absence of extensive alliances among kin, which normally stabilize the rank order, juveniles were able to benefit from infrequent, opportunistic interventions by high-ranking nonkin individuals.     

Aggressive and neutral interventions in conflicts in captive groups of brown lemurs (Eulemur fulvus fulvus)

Third-party interventions in conflicts have revealed complexity in primate social relationships. This type of intervention has seldom been analyzed in prosimians, although many of these species exhibit complex (multimale/multifemale) social organizations. The present study on captive brown lemurs (Eulemur fulvus fulvus) shows that dominant individuals were more likely to intervene in conflicts. Both males and females intervened aggressively in conflicts. Female aggressive interventions occurred mainly on behalf of close kin, whereas males mainly intervened on behalf of juveniles. This study also provides the first record of neutral or peaceful interventions in lemurs. Although females intervened neutrally, almost all neutral interventions were by dominant males. Dominant males intervened in conflicts neutrally more often than aggressively, principally in conflicts between adults and juveniles or between juveniles. Neutral interventions by males always ended the conflicts and were often followed by affiliative contacts between participants (intervenors and opponents). In lemurs, female interventions can be explained by kin selection, while the nature of dominant males' interventions suggests a control role. Interventions by males on behalf of juveniles may increase the formers' fitness.     

雌性黄山短尾猴回避近亲交配

本研究分别在交配期(2006年9月-2006年12月)和产仔期(2007年1月-2007年4月)对黄山短尾猴鱼鳞坑YA1群中5只雄猴和5只雌猴成年个体采用目标动物法、随机取样法和连续记录法记录行为参数。研究期间记录交配行为336例:母子交配0例;母系兄妹交配7例(占2.1%),其中强行交配4例;非亲缘关系交配329例(占97.9%),非亲缘关系交配频次显著高于亲缘关系。在交配期,雄猴对亲缘雌猴跟随、性检查频次均低于非亲缘雌猴,接近指数(PMI)在亲缘和非亲缘雌猴间无显著性差异;雌猴对亲缘雄猴交配拒绝率显著高于非亲缘雄猴,接近指数在交配期显著低于非亲缘雄猴,产仔期接近指数在亲缘和非亲缘雄猴间无显著性差异。尽管雄猴在交配选择上趋于避免与亲缘雌猴交配,但某些雄猴仍会主动对有亲缘关系的雌猴邀配或强行交配,雌猴则主动回避。这些结果表明:黄山短尾猴母系亲属间可以通过行为倾向抑制近亲交配发生,且雌猴更主动回避交配,支持了近交回避的双亲投资理论。     

Matrilineal rank Inheritance varies with absolute rank in Japanese macaques

In many cercopithecine primates, females form linear dominance hierarchies based on kinship. It is known that female rank follows the rules of matrilineal rank inheritance (MIR): (1) maternal rank inheritance, (2) maternal dominance, and (3) youngest ascendancy among sisters. Although, several determining such variation remain largely unknown. In this paper, I investigate the dominance relation-ships of 69 adult (>6 yr old) female Japanese macaques (Macaca fuscata fuscata) in a free-ranging provisioned troop living in Shiga-Heights (Nagano Prefecture, Japan) and report new evidence of intra-group variation. Dominance relationships among high-ranking females followed MRI within kin units, those among low-ranking females did not. Maternal rank inheritance and youngest ascendancy operated between mother/daughter dyads and sister dyads of high-rank, but not in the dyads of low-rank. The dominance ranks of females from low-ranking kin units were dispersed and less predictable. These findings suggest that MRI varies with absolute dominance rank, and are discussed in relation to other asymmetries between high-and low-rank     

Female rhesus macaques discriminate unfamiliar paternal sisters in playback experiments: support for acoustic phenotype matching

Widespread evidence exists that when relatives live together, kinship plays a central role in shaping the evolution of social behaviour. Previous studies showed that female rhesus macaques (Macaca mulatta) recognize familiar maternal kin using vocal cues. Recognizing paternal kin might, however, be more difficult as rhesus females mate promiscuously during the possible conception period, most probably concealing paternity. Behavioural observations indicate that semi free-ranging female rhesus macaques prefer to associate with their paternal half-sisters in comparison to unrelated females within the same group, particularly when born within the same age cohort. However, the cues and mechanism/s used in paternal kin discrimination remain under debate. Here, we investigated whether female rhesus macaques use the acoustic modality to discriminate between paternal half-sisters and non-kin, and tested familiarity and phenotype matching as the underlying mechanisms. We found that test females responded more often to calls of paternal half-sisters compared with calls of unrelated females, and that this discrimination ability was independent of the level of familiarity between callers and test females, which provides, to our knowledge, the first evidence for acoustic phenotype matching. Our study strengthens the evidence that female rhesus macaques can recognize their paternal kin, and that vocalizations are used as a cue.     

The effect of solicitations on grooming exchanges among female Japanese macaques at Katsuyama

In group-living primates, individuals often exchange grooming with not only kin but also non-kin. We investigated the effect of soliciting behaviors on grooming exchanges in a free-ranging Japanese macaque (Macaca fuscata) group at Katsuyama. In this study, we used a focal animal sampling method, targeting 14 females. Data were collected for 15.75 ± 2.67 (mean ± SD) hours per focal female. We classified female–female pairs into three pair types: kin pairs, affiliated non-kin pairs, and unaffiliated non-kin pairs. Females received grooming more frequently when they solicited after grooming their partners than when they did not solicit in all pair types. In addition, females received grooming less frequently when they did not groom their unaffiliated non-kin partners before soliciting; prior grooming was not needed to receive grooming from kin or affiliated non-kin partners. The degree of grooming reciprocity did not differ according to the frequency with which females in kin or affiliated non-kin pairs solicited after grooming. On the other hand, grooming reciprocity between unaffiliated non-kin females was more balanced when they solicited frequently after grooming, as compared with when they did not. In conclusion, our study suggests that soliciting behaviors promote grooming exchanges in female Japanese macaques.     

Long-Term Trends in Matrilineal Inbreeding Among the Japanese Macaques of Arashiyama B Troop

In a long-term study of sexual behavior in Japanese macaques, we found that matrilineal inbreeding accounted for 2.9% of the copulations recorded for the Arashiyama B troop during 7 mating seasons between 1968 and 1984. Of the 906 copulatory dyads, 46 (5.1%) occurred among kin. Close matrilineal kin dyads (r = 1/2–1/8, 1.1% of the total of copulatory dyads) strongly avoided matrilineal inbreeding, but for remote kin dyads (r > 1/8, 4.0% of the total) the tendency was weaker in some years. Among the possible determinants of matrilineal inbreeding, we found that it tended to occur among younger and lower-ranking males as an effect of troop demographic changes. There is no significant association between female rank and matrilineal inbreeding. Our results are consistent with the hypothesis that different degrees of kin relatedness are discriminated by individuals with respect to mate choice.     

Kinship Bonds Are Not Necessary for Maintaining Matrilineal Rank in Captive Japanese Macaques

Although kinship is of central importance in matrilineal (nepotistic) dominance systems, various lines of evidence indicate that its role has probably been overestimated. For example, alliances among nonkin, patterned on the basis of dominance per se, contribute to the maintenance of rank and to the remarkable stability of matrilineal rank orders. But because kin and nonkin alliances exert their stabilizing effects on the rank order simultaneously, the effect of nonkin alliances per se is unknown. We tested whether nonkin alliances are sufficient to ensure the stability of matrilineal rank relations in a laboratory-housed group of Japanese macaques (Macaca fuscata). We first created a group composed of two female subgroups: (1) a subordinate subgroup of close kin known to constitute an effective revolutionary alliance and (2) a dominant subgroup composed mostly of nonkin and distant kin known to support each other against lower-ranking females. In the course of 12 consecutive experimental manipulations, we reduced progressively the relative power of the dominant subgroup by manipulating its size and age composition. The members of the dominant subgroup maintained their rank in all experimental situations except when alone. Thus, nonkin alliances remained effective up to extremely pronounced levels of power imbalance. These results suggest that the remarkable stability of matrilineal rank orders is not conditional upon the existence of nepotistic alliances and strong matrilines of close kin.     

Determinants of male mating success in a large group of Barbary macaques (Macaca sylvanus) at Affenberg Salem

Male mating activities in relation to the likelihood of ovulation and conception were studied in a large group of semifree-ranging Barbary macaques (Macaca sylvanus) during two successive mating seasons. In both mating seasons, adult males attained a significantly higher mating success than subadult males, and they monopolized high ranking females more effectively than low ranking females during the period when conception was most probable. Also, in both mating seasons male rank was significantly correlated with male mating success if all sexually mature males were included. Nevertheless, mating success was not a linear function of age or rank. In both mating seasons mating success of 5-year-old males was much higher than that of dominant but peripheralized 6- and 7-year-old males. Moreover, a significant correlation between rank and measures of mating success among adult males was found in the second but not in the first mating season. The results indicate that mating and, most probably, reproductive success of male Barbary macaques is dependent on the male's social position in the group, which is defined not only by the outcome of dyadic agonistic encounters but also by the ability to get a central position in the group, and on the stability of rank relations.     

Rank relations of juvenile and subadult natal males of Barbary macaques (Macaca sylvanus) at Affenberg Salem

Rank relations of more than 100 juvenile and subadult natal Barbary macaque males were analyzed. Hierarchical relations among individuals of the same age were established early during the first year of life. With few exceptions concerning infants from very high-ranking genealogies, males dominated female peers regardless of maternal rank. Males started to outrank females from older cohorts during the second year of life and completed the process of rank reversal with adult females at 5-6 years of age. An age-graded dominance pattern existed among males from different birth cohorts. Only 3 rank reversals between males from different cohorts were observed. Rank reversals among males of the same birth cohort occurred more frequently. Rank position of a male among his male peers was influenced by birth order, by maternal rank, and by the presence of juvenile brothers. Most males without juvenile brothers had low positions, regardless of maternal rank. Males born late in the birth season were also low-ranking, even when juvenile brothers were present. There was no cohort where ranking among males was determined by maternal rank alone, as is the case in rhesus monkeys and Japanese macaques. Adult/subadult male carriers had no noticeable effect on rank positions of 'their' infants. It is suggested that a weaker influence of Barbary macaque mothers on rank of their sons is related to very early integration of male infants in male social/play groups.     

Male and Female Reproductive Success in <Emphasis Type="Italic">Macaca sylvanus</Emphasis> in Gibraltar: No Evidence for Rank Dependence

The relationship between social rank and reproductive success is one of the key questions for understanding differences in primate social group structures. We determined the paternity of 18 infants in a social group of Barbary macaques (Macaca sylvanus) born over a period of 6 yr in the provisioned, free-ranging colony in Gibraltar. We successfully used 13 pairs of primers of variable microsatellite loci to amplify DNA from blood and hair samples and applied the computer programs CERVUS 2.0 and KINSHIP 1.3 to assign paternity to 13 candidate males. We collected data for 19 females that had given birth to 66 infants over a period of 7 yr. We used paternity analyses and female birth records to test the hypothesis that social rank is correlated with reproductive success. Results showed that numbers of paternities and maternities were equally distributed among all reproducing individuals in the social group regardless of rank. Subadult males reproduced as often as adult males. High-ranking females did not start to reproduce earlier than low-ranking females. Interestingly, there was a tendency toward a positive correlation between the ranks of mothers and the ranks of the corresponding fathers. It might be concluded either that a correlation between social rank and reproductive success is generally absent in Barbary macaques or that artificially favorable environmental conditions in Gibraltar preclude any correlation between social rank and reproductive success.     

Function and distribution of coalitions in captive bonobos (Pan paniscus)

We examined the distribution of support behaviour within a captive group of bonobos. Most support was evoked by inter-sexual conflicts with the two highest ranking females. Within a dyad, the usual winner was most often supported. Individuals that challenged the rank order by aggressions and pestering were aggressed more often by their targets in the company of an ally. The two lowest ranking males served as scapegoats, receiving 80% of the contra-support. In coalitions, inviduals did not aggress victims they would not dare to attack without supporters. However, the victims of coalitions reacted more strongly with fear and rarely counteraggressed than when being attacked alone, indicative of the high impact of aggression in support. The alpha female showed some control behaviour when intervening in conflicts. The data fitted with several functional hypotheses: coalitions functioned to maintain existing ranks, to acquire ranks, to reduce tension, and to test or strengthen the bond. We suggest that support behaviour fulfilled a crucial role in the maintenance of the power of the two highest ranking females over the males. Among the females themselves the dominance relationships were not based on coalitions, but on individual attributes.     

Dyadic and triadic reconciliation in pigtail macaques (Macaca nemestrina)

The tendency in primates for former antagonists to approach and affiliate following aggression has been termed reconciliation because the response is thought to resolve social conflicts produced by aggression. In primate societies, however, an aggressive interaction between two individuals often spreads to include other group members, especially the kin of the combatants. If post conflict affiliation resolves aggressive conflicts in a group, then affiliative increases might occur between combatants and the kin of their opponents following aggression as well as between former opponents. This hypothesis was tested in a captive group of 39 pigtail macaques (Macaca nemestrina) by comparing affiliative response frequencies of combatants during the 5 minute period following aggression to affiliative response frequencies during 5 minute baseline periods not preceded by aggressive activity. Following aggression, affiliation rates increased between combatants and their opponents, aggressors and the kin of their opponents, and aggressors and their own kin. Additional analyses showed that aggression among kin was reconciled more often than aggression among nonkin. Recipients of aggression reconciled with their attackers more often than aggressors reconciled with their victims. Animals with similar dominance ranks reconciled proportionately more often than those with large rank disparities and aggressive infractions of a calculated dominance hierarchy were reconciled more often than attacks consistent with the hierarchy. Results suggest that both dyadic and triadic reconciliations occur in M. nemestrina and that compared to other primate species M. nemestrina exhibit a moderate-to-high conciliatory tendency.     

Post-conflict Behaviour of Wild Olive Baboons. I. Reconciliation,Redirection and Consolation

Observations of post-conflict interactions have provided important insights into primate social organization. In this study, the nature and determinants of post-conflict behaviour in a troop of wild olive baboons, Papio anubis, were investigated. Reconciliation was observed among all age-sex classes, occurring at a rate consistent with a relatively intolerant dominance style. Reconciliation was more frequent when one of the combatants carried a dependent infant but rarely followed conflicts associated with food. Neither the directionality nor the decidedness of conflicts affected conciliatory tendency. In contrast, opponents that were close kin or of similar rank reconciled more often. Olive baboons did not affiliate with non-combatants more frequently following aggression than in control periods, although affiliation with supporters and the close kin of opponents increased. Absence of consolation follows the observed cercopithecine pattern, consistent with the hypothesis that consolation requires an ability to empathize with the victim's distress. Initiation of post-conflict attacks on third parties was not elevated in victims of aggression. The rarity of redirection is attributed to spatial dispersion, the frequent bidirectionality of baboon aggression and regular male intervention in female conflicts, all of which appear to limit the availability of ‘safe’ targets.     

The function of Barbary macaque copulation calls.

In a wide variety of animal species, females produce vocalizations specific to mating contexts. It has been proposed that these copulation calls function to incite males to compete for access to the calling female. Two separate advantages of inciting male-male competition in this way have been put forward. The first suggests that as a result of calling, females are only mated by the highest ranking male in the vicinity (indirect mate choice hypothesis). The second proposes that copulation calling results in a female being mated by many males, thus promoting competition at the level of sperm (sperm competition hypothesis). In this paper, I give results from the first experimental study to test these hypotheses. Playback was used to examine the function of copulation calls of female Barbary macaques (Macaca sylvanus) in Gibraltar. Although rank did not affect lone males'' likelihood of approaching copulation calls, when playbacks were given to pairs of males only the higher ranking individual approached. Moreover, females were mated significantly sooner after playback of their copulation call than after playback of a control stimulus. These results suggest that the copulation calls of female Barbary macaques play a key role in affecting patterns of male reproductive behaviour, not only providing an indirect mechanism of female choice, but also promoting sperm competition by reducing the interval between copulations. Potential fitness benefits of inciting male-male competition at these two levels are discussed.     

Sex Ratio Adjustment in a Seasonally Breeding Primate Species: Evidence from the Barbary Macaque Population at Affenberg Salem

Presented are data on secondary sex ratio in a large population of semifree-ranging Barbary macaques (Macaca sylvanus) at Affenberg Salem. Examined were 569 births in five social groups with regard to demographic parameters, maternal age and rank. Significant differences were found between the secondary sex ratios of high ranking and low ranking females. A higher proportion of male offspring was born in the high ranking class, while both groups did not differ in fecundity rates. A detailed analysis of the reproductive cycles of 73 females showed a significant shorter interval between the end of conceptional estrus and birth in male infants and also a significantly earlier onset of deturgescence of anogenital swelling when males were conceived. These results strongly suggest that the differences in the secondary sex ratio are not due to differential abortions but rather to pre-conceptional control of sex via timing of mating in relation to ovulation.     

A matrilineal overthrow with destructive aggression inMacaca fascicularis

We report the sequence of a matrilineal overthrow in longtailed macaques (Macaca fascicularis) during which the α-matriline dropped to the third of four ranks. In the initial phase of the overthrow, females from the former second ranking matriline attacked the females of the former α-matriline in a sequence which suggests a strategy. They attacked the highest ranking mother first and then directed their attacks toward her daughter, then toward her grand-daughter, and finally toward her great-grand-daughter. This seems to be the most effective way to disrupt the possible interventions of mothers in favor of their daughters.     

Social behavior of infant and mother Japanese Macaques (Macaca fuscata): Effects of kinship,partner sex,and infant sex

The behavioral interactions of 22 infant and mother Japanese macaques with other group members were studied. Focal-animal observations were made from the time of each infant’s birth until 1 year of age. Infants and mothers both displayed exceedingly strong preferences for associating with matrilineal kin and, specifically, for female kin. The degree of genetic relatedness was positively correlated with levels of spatial proximity, contact, grooming, aggression, and play. Overall frequencies of interactions with nonkin were very low, and partner sex was not an important factor in interactions with nonkin. There were no significant differences between male and female infants in interactions with kin versus nonkin. There was only one significant difference between male and female infants in interactions with males versus females: female infants showed stronger preferences for initiating proximity with females over males than did male infants. Because mothers provide the focal point for infant interactions during the first year of life, we compared the behavior of infants and mothers. Mothers were the recipients of more social interactions than were infants, mothers engaged in more grooming than did infants, and infants engaged in more social play than did mothers. These findings are only partially consistent with kin-selection theory, and the inadequacies of studying matrilineal kin discrimination to test kin selection are reviewed. The near-absence of infant sex differences in associations with social partners suggests that although maternal kin other than the mother are important to infant socialization, they probably do not contribute to the development of behavioral sex differences until after the first year of life.