Reproductive senescence and terminal investment in female Barbary macaques (Macaca sylvanus) at Salem

The reproductive history of 207 female Barbary macaques, living in a large outdoor enclosure in Southwest Germany, was studied during an 11-year period. The results yielded a significant relationship between female age and fecundity, with fertility rates lower than expected among young and old females. Analysis of the reproductive history of individual females revealed a significant decline in fertility from prime age (7–12 years) to mid age (13–19 years), and from mid age to old age (20–25 years). The proportion of long interbirth intervals increased steadily among aging females. Infant survival was not significantly related to maternal age, but offspring of old females showed the highest survivorship. Behavioral observations revealed that old mothers weaned their offspring significantly later than younger mothers, suggesting that prolongation of interbirth intervals is due not only to deteriorating physical condition but also to increased maternal investment, as life history theory predicts. Reproduction ceased during the middle of the third decade of life. Final cessation of estrous cycling invariably occurred 3 or 4 years after the birth of the last offspring, but a postreproductive life span of 5 years appears to be common in this population. Available data suggest that reproductive senescence and menopause are more common among nonhuman primates than widely believed and that both traits are part of an adaptive life history strategy.     

Dynamics of fission in a wild Barbary macaque group (Macaca sylvanus)

We studied the dynamics of a group of Barbary macaques (Macaca sylvanus) in Algeria from March 1983 to November 1989. Troop fission began in autumn 1987, when group size had more than doubled, to include 76 animals. We observed 11 temporary splits of this group during the mating seasons of 1987 and 1988. The process was interrupted during the 1988 birth season. In June 1989, fission resumed and ended with the formation of three independent groups that included 50, 24, and 13 individuals. Adult females played an important role in the process of fission. They initiated the rapid formation of two, and later three, coherent nuclei, distributed in two or three bisexual subgroups; on several occasions these nuclei also formed subgroups without any adult males. Adult males remained together in a single nucleus for longer periods of time than females did. However, during fission, 35% (N=20) of resident males emigrated to neighboring groups, while 11 strange males immigrated into the focal group; over 6 years, 57% of the male transfers occurred after the beginning of the process. After group fission, maternally related individuals lived together in the new groups. The majority of resident males remained with the largest of the three groups, while most of the immigrant males were in another group. The third group included a single adult male. Possible factors that induce group fission are discussed.     

Group Fission in Barbary Macaques (Macaca sylvanus) at Affenberg Salem

We analyzed eight group fissions occurring during a 20-year period in three groups of a free-ranging provisioned Barbary macaque population. The founder group fissioned four times within 3.5 years after transfer to the enclosure, indicating that external factors—new environment, more space, absence of other groups—facilitated group fissions. Two groups resulting from these fissions, split twice within 2.5 and 1 years, respectively, many years later. The process of fissioning lasted from a few months to almost 2 years. Fissions were preceded by peripheralization/subgrouping of mainly young adult males (8-10 years old), suggesting that male competition was the primary force for the fissions. The males were joined by middle- to low-ranking but not the lowest-ranking females. The resulting new groups were usually smaller than the groups in which the former -matriline—old groups—stayed, and they were also more variable in size and sex ratio, suggesting that variable numbers of surplus individuals were expelled during fission. Mean adult sex ratios were similar in both groups after fission, indicating that the competitively superior males in the old groups (groups + -matriline) could not increase their breeding opportunities. Female kin, even of large matrilinies, almost always stayed together during fission. Natal males strongly preferred to join the old groups, and this preference was most pronounced in juveniles and subadults. Hence, most natal males stayed with maternally related females, i.e., remained true natal males, if the females stayed in old groups. They were separated from female kin, i.e., became seminatal, if the females joined the new groups. These seminatal males did not differ from natal males with respect to matrilineal rank, but they had more female relatives, above all more close relatives (sisters), indicating that avoidance of mating with maternal kin was important for group choice. Despite joining the same group as female kin during fissioning, breeding opportunities of natal males (ratio of unrelated females/male) were not less than that of their seminatal peers, because natal males had fewer female relatives. Only a minority of both groups of males would have done better by joining the alternative group. Paternal relatives were distributed during fission by chance, and loss of patrilinies was therefore much less pronounced. We conclude that the rules governing social relationships among Barbary macaque males are less apt to cope with the high number of males resulting from provisioning, whereas the rules regulating social relationships of females living in a nepotistic, female-bonded society are very robust in this respect.     

Sexual behavior of wild Barbary macaque males (Macaca sylvanus)

Recent assertions that the Barbary macaque (Macaca sylvanus) is a multiple-or serial-mounting species are incorrect. Data are presented from over 300 copulations observed among wild Moroccan Barbary macaques which establish empirically that males of this macaque species are single mounters. The average length of an ejaculatory copulation was 8.7 sec, with a range of 6 to 14 sec. Ejaculation occurred an average of 6.3 sec after mounting, with an average of nine pelvic thrusts per ejaculation. Males appeared capable of ejaculating twice within 16 min, and three consecutive times within 37 min. Characteristically, only one mount and ejaculation occurred during a sexual association between an estrous female and each of her consorting males. Schemes of macaque evolution which incorrectly classify Barbary macaques as a multiple-mounting species should be viewed cautiously.     

Maternal discrimination of offspring vocalizations in Barbary macaques (Macaca sylvanus)

The response of Barbary macaque (Macaca sylvanus) females to vocalizations of their offspring was studied in a semi-free ranging population. The results of both facal observations and playback experiments demonstrated that mothers preferentially turned to their offspring's vocalizations over those of other young, providing evidence that mothers are able to recognize their offspring by acoustic signals alone. We assume that they may use this ability to monitor their infants' activities.     

Group fission in a semifree-ranging population of Barbary macaques (Macaca sylvanus)

During a 16-month study of semifree-ranging Barbary macaques (Macaca sylvanus) the group under observation divided into two groups. Observations were carried out in 1987–1988, at «La Montagne des Singes,” Kintzheim, France. A subgroup of monkeys, which was already cohesive at the beginning of the study, became progressively autonomous in relation to the rest of the main group, during the mating season. Overt aggression between the males of the two groups during this period brought about the fission. Only low-ranking genealogies left their group of origin. Dominance relations between females remained identical in both groups except for one lineage. The alpha male and the alpha female of the subgroup had a close relationship before the fission occurred. The sequence of agonistic intergroup relations is described and analyzed in relation to male sexual competition and female alliance power. The results suggest that: (1) the males of the subgroup instigated the fission because it was the best strategy for them to counter sexual competition; and (2) the females followed the males in order to maintain their alliance network, necessary to insure their dominance status over subordinate females.     

The social position of male Barbary macaques (Macaca sylvanus) in a semifree-ranging population

A study was carried out on the social position of 12 subadult males of a semifreeranging Barbary macaque population during the non-mating season. The social position was measured in terms of spatial as well as interactive parameters. The subadult males had social contacts to members of nearly all other age-sex classes but showed clear preferences for same-sexed partners. Besides this differences were found between 5- and 6-year-old males with respect to their interaction profiles and the preference for special classes of interaction partners. The terms “peripheral-central” is discussed with reference to the social structures of macaque societies. The data of the present study indicate that the social position of subadult male Barbary macaques can not be described by one of these terms exclusively. The results are compared to other studies on Barbary macaques and other macaque species. It is concluded that in macaque societies subadult males are not obligatorily forced to live at the periphery or to abide. It is proposed not to postulate stiff social structures but to put more emphasis on the range of variation among macaque species.     

Intergroup transfer and incest avoidance in semifree-ranging barbary macaques (Macaca sylvanus) at Salem (FRG)

During a long-term study of social behavior of semifree-ranging Barbary macaques, data on group transfer and sexual behavior were collected. A large population containing five groups living in a 14.5 ha outdoor enclosure was studied. Demographic data on the whole population are available for a period of six years. Data on sexual behavior of members of one large group were collected, by both focal animal and ad libitum techniques, for a period of two years. Matrilineal kinship relations of all except the oldest members of this intensively studied group were known. Males changed groups most frequently between the ages of three and five years i.e., the time at which sexual maturity was reached. While more than 30% of all males three years old and older changed groups during the study period, many males remained members of their natal group even after reaching adulthood. However, sexual interactions, especially matings between close matrilineal relatives, were found to be almost absent, suggesting that Barbary macaques are not highly inbred as formerly supposed.     

Male Migration in Barbary Macaques (Macaca sylvanus) at Affenberg Salem

We analyzed male migration during a 20-year period in the free-ranging Barbary macaque population of Affenberg Salem. Most natal migrations occurred around puberty, but only one third of all males left the natal group. Secondary group transfers were rare. All males immediately transferred to other bisexual groups. Migration rates were highest during periods with high adult female/male ratios within social groups. Immigrants highly preferred groups with fewer males of their own age than in the natal group, and many males immigrated into groups that had no male their own age. These groups originated from a skewed distribution of resident males during group fissions. A comparison of emigrants with their natal peers supports the inbreeding avoidance hypothesis as cause of emigration rather than the male competition avoidance hypothesis. Emigrants had no lower individual rank position and did not come from lower-ranking matrilines. Emigrants had more female maternal relatives, especially sisters. Males without female relatives almost never emigrated. Conversely, there is virtually no indication that emigrants were evicted from the natal group. Emigrants had no increased mortality. Paternity data revealed that the reproductive success of emigrants and natal males is similar, indicating that emigration had no reproductive cost. Many similarities between emigrants and natal males that separated from female maternal kin during group fissions suggest that inner migration during fissions is an alternative way to avoid maternal inbreeding. The mating system resulted in a genetic structure within social groups that largely diminished the chances for paternal inbreeding even without recognizing paternal kin.     

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.     

The association between rank,mating effort,and reproductive success in male Barbary macaques (Macaca sylvanus)

The association between social rank, mating effort, and reproductive success of male Barbary macaques (Macaca sylvanus) has been evaluated by longterm behavioral observations and subsequent paternity determination via oligonucleotide DNA fingerprinting in a large semifreeranging group. All offspring born between 1985 and 1988 that survived to at least 1 year of age (n=75) were available for paternity testing. The exclusion of all but one of the potential fathers from paternity was possible in 70 cases (93%). Mating activities were recorded using ad lib. and focal female sampling techniques. The analysis of male mating effort was restricted to the most likely days of conception. Male rank correlated significantly with male mating success in all four breeding seasons and with male reproductive success in three of the four seasons. Mating success and reproductive success also showed a significant correlation, with the exception of one breeding season, in which the proportion of males per fertilizable female was especially high. Poor mating success was almost always associated with poor reproductive success, while good mating success was less predictive for a male's actual reproductive success. This was apparently a consequence of sperm competition, resulting from the promiscuous mating system. Male mating success is not necessarily an unreliable indicator for reproductive success, provided that sufficient sample sizes are available and that conception periods can be determined. Sperm competition and other factors may weaken the association, however.     

Male intergroup mobility in a wild population of the Barbary macaque (Macaca sylvanus), Ghomaran rif mountains,Morocco

In this two-year study of a Barbary macaque population (n = 162) in the Ghomaran region of Morocco, 13 cases of males separated from their assumed natal groups were observed (nine visits of nonresident males to groups, two males isolated from groups as much as one day and one night, and two sets of snow tracks indicating males travel +7 km as isolates). Males left their assumed natal groups primarily in the mating season (12 cases), focused their interactions on estrous females of other groups, and were observed to copulate with these females in two cases. All males leaving their assumed natal groups were estimated to be between 5 and 8 years of age, with one exception (+ 15 years). It could not be determined whether males younger than 5 years moved between groups, or whether any males made permanent intergroup transfers. Regardless, the data from this study indicate that male intergroup mobility (and intergroup gene flow) was higher than has been previously assumed for this species. A prior theory that Barbary macaque groups are highly inbred, and that this is causally related to the evolution of male-infant care in this species, is not supported by the data of this study.     

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.     

Comparative density,demography, and ranging behavior of Barbary macaques (Macaca sylvanus) in marginal and prime conifer habitats

A semiisolated study population of 162 Barbary macaques (six groups) inhabiting the Ghomaran fir forests of the Moroccan Rif mountains has a density of 6.73 individuals/km ². The adult sex ratio is 0.725, and immatures comprise 46.9% of the population. Births are seasonal, occurring from April to June, and the adult female birth rate is 0.58 per annum. Mortality appears relatively low in all age classes until old age. Group size ranges from 12 to 59 individuals, with a median value of 24. Home-range sizes vary between 3 and 9 km², with a mean of 7.2 km². Home-range overlap is approximately 80%. On the basis of macaque density, conifer density, and herding competition from domestic animals, the Ghomaran environment can be considered “marginal” compared to the Moyen Atlas. Despite the marginal habitat of the Ghomaran population, it is surprisingly similar in demographic characteristics to a Barbary macaque population in the Moyen Atlas. Two characteristics of the population dynamics in the Ghomara differentiate it from the former. (1) The mean home range is five times larger in the Ghomara, roughly inversely proportional to the sixfold decrease in macaque density, confirming Caldecott’s (1986) principle that, in macaque species, range size adjustments are a primary proximate response to poor-quality habitat. (2) Smaller groups in the marginal habitat of the Ghomara appear to have better rates of growth than small groups in prime habitat. This may result from an overall decreased home-range defensibility in marginal habitat (larger home ranges), resulting in an ecological and demographic release of small groups from the levels of intergroup competition they would normally experience in prime habitat.     

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.     

A fatal attack on an unweaned infant by a non-resident male in a free-ranging group of Japanese macaques (Macaca fuscata) at Katsuyama

A non-resident male attacked a 4-month-old unweaned infant in a free-ranging group of Japanese macaques (Macaca fuscata) and it died 2 days later from a severe wound. When the infant was alone at the feeding site, the non-resident male rushed at it. The infant ran away as soon as it became aware of the male, but was captured. The male bit the infant on its hand, foot, and arm, while continuously scanning his surroundings. He did not kill the infant immediately and, after the infant escaped, he did not chase or attack it at all. Although the infants right arm was bleeding heavily, it survived until the following day. The infanticide occurred a few weeks before the mating season began, so the victims mother soon resumed estrus and the subsequent inter-birth interval was shortened. The first-, second-, and fourth-ranking adult males had died or disappeared a few months before this infanticide, and there were no other group members near the infant when the infanticidal male appeared. The infanticidal male had not been observed before this incident. Compared to one-male groups, the occurrence of infanticide in multi-male groups of Japanese macaques is extremely infrequent. However, in other reports of infanticide in Japanese macaques as well as in this case, it has been noted that infanticide is likely to occur in the pre- or early-mating season, when there are no resident males to defend the infant against attacks, and when a threatening male is least likely to be the infants father.Electronic Supplementary Material Supplementary material is available for this article at     

Exploring the components, asymmetry and distribution of relationship quality in wild Barbary macaques (Macaca sylvanus)

Social relationships between group members are a key feature of many animal societies. The quality of social relationships has been described by three main components: value, compatibility and security, based on the benefits, tenure and stability of social exchanges. We aimed to analyse whether this three component structure could be used to describe the quality of social relationships in wild Barbary macaques (Macaca sylvanus). Moreover, we examined whether relationship quality was affected by the sex, age and rank differences between social partners, and investigated the asymmetric nature of social relationships. We collected over 1,900 hours of focal data on seven behavioural variables measuring relationship quality, and used principal component analysis to investigate how these variables clustered together. We found that relationship quality in wild Barbary macaques can be described by a three component structure that represents the value, compatibility and security of a relationship. Female-female dyads had more valuable relationships and same-age dyads more compatible relationships than any other dyad. Rank difference had no effect on the quality of a social relationship. Finally, we found a high degree of asymmetry in how members of a dyad exchange social behaviour. We argue that the asymmetry of social relationships should be taken into account when exploring the pattern and function of social behaviour in animal societies.     

Demography and reproductive parameters of a free-ranging group of Japanese macaques (Macaca fuscata) at Katsuyama

Demographic and reproductive data were analyzed for a period of 28 years in the females of a free-ranging group of Japanese macaques at Katsuyama, Okayama Prefecture, Japan. The overall mean, age-specific fecundity rates were 5.43% for 4-year-olds and 41.86% for 5-year-olds, increasing to a peak of 66.67% for 13-year-olds. Fecundity remained relatively high (52.31–54.24%) in 16–19-year-olds, but decreased sharply (45.45–17.86%) in 20–23-year-olds, and became very low in 24–26-year-olds. Females aged 27 years or more did not produce infants. The average age at first birth was 5.41 years. Births peaked in mid-May. The timing of the first births each year remained essentially unchanged during the study period, whereas the timing of the median and last births shifted towards the later part of the season. The mean interbirth interval for all females was 1.56 years. The value was 1.54 years for multiparous females and 1.29 years for females following infant loss. These intervals were significantly shorter than those for primiparous females, and females with surviving infants. The overall mean infant mortality within the first year of life was 10.2%. The value was 8.6% for 10–14-year-olds, and 7.5% for 15–19-year-olds. The timing of birth differed among the four female matrilineal dominance rank-classes. The female fecundity rates increased as a function of matrilineal dominance rank. It is suggested that all demographic and reproductive data should be analyzed in detail with respect to the group's history.     

Frequent harassment of mounting after a takeover of a group of moor macaques (Macaca maurus)

Harassment behavior during mounting was observed in a group of moor macaques (Macaca maurus) in Sulawesi, Indonesia. During the study periods in 1994 and 1995, most harassment was performed by juveniles less than 5 years old. No harassment by adult females was observed. Mounting by the α-male, who had newly immigrated to the group, was harassed more frequently than that by the β-male in 1994. In 1995, the frequency of harassment during mounting by the α-male was low as compared with that in 1994. In the case of the new α-male, harassment occurred more frequently during mounting with sexually tumescent females than during mounting with detumescent females. Harassment was rarely observed during mounting by natal males of the group. Many hypotheses have been proposed to explain harassment of mounting in primates. The present results offer support for the following two hypotheses: (1) harassment is an attempt to establish a social bond between the performer and the mounting individuals; or (2) harassment occurs in response to mounting by unfamiliar males.