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.     

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.     

Concealing of facial expressions by a wild Barbary macaque (Macaca sylvanus)

Behavioural research on non-vocal communication among non-human primates and its possible links to the origin of human language is a long-standing research topic. Because human language is under voluntary control, it is of interest whether this is also true for any communicative signals of other species. It has been argued that the behaviour of hiding a facial expression with one’s hand supports the idea that gestures might be under more voluntary control than facial expressions among non-human primates, and it has also been interpreted as a sign of intentionality. So far, the behaviour has only been reported twice, for single gorilla and chimpanzee individuals, both in captivity. Here, we report the first observation of concealing of facial expressions by a monkey, a Barbary macaque (Macaca sylvanus), living in the wild. On eight separate occasions between 2009 and 2011 an adult male was filmed concealing two different facial expressions associated with play and aggression (“play face” and “scream face”), 22 times in total. The videos were analysed in detail, including gaze direction, hand usage, duration, and individuals present. This male was the only individual in his group to manifest this behaviour, which always occurred in the presence of a dominant male. Several possible interpretations of the function of the behaviour are discussed. The observations in this study indicate that the gestural communication and cognitive abilities of monkeys warrant more research attention.     

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.     

Food resources of the wild Barbary macaque (Macaca sylvanus) in high-altitude fir forest, Ghomaran Rif, Morocco

A small geographically isolated population of the Barbary macaque inhabits a high-altitude fir forest habitat ( Abies pinsapo ) in the Ghomaran region of the Rif mountains of northern Morocco. The climate of this region is Mediterranean, but the altitude (1600–2100 m) causes winters to be cold (as low as -8.0 C) with snow occurring from November to May (snowfall as deep as 1.5 m). The primary winter feeding adaptation is the ability to ingest high quantities of fir foliage; in spring, the macaques took a high diversity of leafy food items from all vegetation layers; in summer, the macaques foraged terrestrially for a high diversity of food items including seeds, small fruits, bulbous geophytes, and animal foods (including tadpoles from small streams); in autumn, the macaques returned to arboreal foraging, primarily feeding on oak acorns ( Quercus ilex ), fir seeds and yew fruit ( Taxus baccata ). The macaques were capable of ingesting 100 of 195 (51%) of all identified plant species in the region, although during the four-month winter, the macaques only averaged 12.5 common food items. A comparison of the study area with the prime habitat of the Barbary macaque-the high-altitude cedar forests of the Moroccan Moyen Atlas-indicates that climate and vegetation physiognomy are highly similar in both regions. Correspondingly, there is a high degree of similarity in macaque diet in both regions in terms of feeding behaviour by season, food diversity and specific feeding techniques. In the Ghomara, the winter feeding adaptation of fir foliage eating parallels that of the Barbary macaque in cedar forest (winter foraging for cedar foliage). This enables the Barbary macaque to exploit the Ghomaran fir forest habitat during the cold, snowy winters much the same as it does cedar forest habitat throughout a major portion of its geographical range.     

Coping with the cold: predictors of survival in wild Barbary macaques,Macaca sylvanus

We report the death of 30 wild Barbary macaques, living in two groups, during an exceptionally cold and snowy winter in the Middle Atlas Mountains, Morocco. We examined whether an individual''s time spent feeding, the quality and number of its social relationships, sex and rank predicted whether it survived the winter or not. The time an individual spent feeding and the number of social relationships that an individual had in the group were positive and significant predictors of survival. This is the first study to show that the degree of sociality affects an individual''s chance of survival following extreme environmental conditions. Our findings support the view that sociality is directly related to an individual''s fitness, and that factors promoting the establishment and maintenance of social relationships are favoured by natural selection.     

Perineal swellings: a social and endocrine advantage for Barbary macaque females (Macaca sylvanus)

This study focuses the relationship between social rank, intersexual behavior, age, fecal cortisol equivalent excretion rates and perineal swelling size in contraceptive-treated Macaca sylvanus females. Behavioral data and fecal samples were collected during a twenty-week period from 24 females. Females were categorized with regard to perineal swelling (enlarged or reduced), and to their dominance rank (high or low); we found that swelling size was not associated with it. However, females with an enlarged perineum received more male grooming interactions, had closer spatial relations to males, and received significantly more interventions from males than did the others. Endocrinologically, females with enlarged swelling showed decreased fecal cortisol equivalent excretion rates. Multiple regression models showed a positive relationship between the extent of the swelling size and grooming, inspection and spatial relation. There was a negative relationship between the extent of swelling size and fecal cortisol equivalents. These results imply that enlarged perineal swellings among implanted Barbary macaque females have a greater impact on intersexual contact and adrenocortical activity than does social rank or age.     

Complex patterns of grooming and sexual activity in Barbary macaques (Macaca sylvanus)

Grooming in primates is often considered a “currency” that can be exchanged for other “services” or “commodities” such as reciprocal grooming, coalitionary support, infant handling, tolerance around food sources, active food sharing, or mating opportunities. Previous studies on primate grooming‐for‐sex exchange viewed the males as the demanding class, with the females as suppliers of mating opportunities. In this study, we examine the broader context of grooming‐for‐mating exchange in Barbary macaques in Gibraltar. Our data show that Barbary macaque males groom females with whom they are mating more frequently and for longer periods than other females, and the relationship between grooming and mating remains significant in both sexual and nonsexual contexts. In addition, females groomed males with whom they were mating more frequently and for longer periods than other males. In both sexes, grooming was observed to be far more frequent and to occur for longer durations in sexual compared to nonsexual contexts. We did not find any difference in grooming behavior between presexual and postsexual contexts. Our data suggest that there is no simple model to describe Barbary macaque grooming patterns in sexual contexts. Although our results are partly consistent with male use of grooming as payment for mating, broadly assessed grooming‐mating patterns cannot be solely explained by a male‐driven grooming‐for‐mating exchange.     

Intergroup interactions in wild Barbary macaques (Macaca sylvanus), Ghomaran Rif mountains,Morocco

Data are presented on intergroup interactions between six groups of Macaca sylvanus in the Ghomaran region of the Moroccan Rif mountains. Intergroup encounters (0.026/observation hour) were defined as two groups being near each other (< 150 m). Encounters were further classified into: 1) neutral (indeterminate) encounters, in which very little intergroup interaction took place, with the exception of male monitoring (N = 7); 2) approach-retreat encounters with intergroup displacement, in which, without any overt agonism, members of one group slowly approached another and caused it to retreat (N = 3); and 3) agonistic encounters with intergroup displacement (N = 3). These results are compared to the only other study of intergroup interactions in wild Barbary macaques, and it is concluded that 1) observations of intergroup unification and/or coordination of movement in Barbary macaques (“herding”) probably resulted from observer error, or if these phenomena do occur, they are rare throughout the range of this species; 2) approximately half of all intergroup encounters in both studies resulted in intergroup displacement and/or intergroup agonism, evidence of intergroup competition; and 3) current data on intergroup interactions in Barbary macaques conform to the predictions of Wrangham's model of mutually competitive female-bonded, multimale groups.     

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.     

The function of teeth chattering in male Barbary macaques (Macaca sylvanus)

Teeth chattering is seen in many primate species and has been proposed to have a range of social functions. This observational study tested specific hypotheses relating to the function of teeth chattering in a semi-free-ranging group of Barbary macaques, Macaca sylvanus. During focal watches of males, the outcome of male-male dyadic social interactions in which teeth chattering was present or absent was compared. Using these data, we tested the predictions of four hypotheses: teeth chattering functions as a signal of submission, appeasement, affiliation or reassurance. Support was found for all four hypotheses. In addition, in some contexts, an exchange of teeth chattering appeared to have a greater impact on the outcome of interactions than one male alone giving this signal. These findings suggest that teeth chattering serves an important role in coordinating the social interactions of male Barbary macaques.     

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.     

Female Barbary macaque (Macaca sylvanus) copulation calls do not reveal the fertile phase but influence mating outcome

In a number of primate species, females utter loud and distinctive calls during mating. Here we aim to clarify the information content and function of Barbary macaque (Macaca sylvanus) copulation calls by testing (i) whether or not copulation calls advertise the female fertile phase and (ii) whether and how copulation calls influence male ejaculatory behaviour. In order to do this, we combined hormone measurements with acoustic analysis and behavioural observations. In contrast to a previous study implying that the structure of copulation calls indicates the timing of the fertile phase, our results, using objective endocrine criteria for assessing ovulation, provide evidence that the structure of copulation calls of female Barbary macaques does not reveal the timing of the fertile phase. More importantly, females seem to influence the likelihood of ejaculation by calling versus remaining silent and by adjusting the timing of call onset. Females make use of this ability to influence mating outcome to ensure ejaculatory matings with almost all males in the group. In addition, calls given during ejaculatory copulations differ from those during non-ejaculatory copulations, providing information about mating outcome for listeners. We conclude that in this species, copulation calls apparently serve to enhance sperm competition and maximize paternity confusion.