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.     

Allogrooming in two species of macaque (Macaca nemestrina andMacaca radiata)

This paper analyzes allogrooming (social grooming) data collected from two large, fully integrated and long established social groups of macaques (one of pigtail macaques and one of bonnet macaques). The data demonstrates a species and sex difference for total allogrooming given with females of both species giving more grooming than the males and with pigtails as a species giving more grooming than bonnets. Also, pigtail females gave more allogrooming to clan members than to nonclan members, but this was not true for pigtail males, bonnet males, and bonnet females. Allogrooming given and allogrooming received by age class for both species showed development of a sexual dichotomy at three to four years. The analysis characterized some of the social structures extant in two closely related species of macaque, particularly the somewhat different use of allogrooming in pigtail females as opposed to the other three categories of animals. Social implications with relation to macaque societies are discussed.     

Female ovarian cycle phase affects the timing of male sexual activity in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar

Although all macaques have a multimale multifemale mating system, the degree of promiscuity shown by the Barbary macaque is considered to be extreme in terms of both mating frequency and number of mating partners. How mating activity is distributed throughout the female menstrual cycle and whether or not copulations are concentrated around the fertile phase as in other members of the genus is, however, not known. To examine this, we collected data on rates of copulation throughout 29 ovarian cycles from 13 free-ranging females of the Gibraltar Barbary macaque population and related them to the time of ovulation and the female fertile phase as determined from fecal hormone analysis. In addition, patterns of male inspection of females and time spent in consortship, both indicators of female attractivity, were also analyzed. The results indicate that both mating behavior and female attractivity vary predictably with ovarian cycle stage. Rates of copulation were found to increase toward the time of ovulation, with a distinct peak of ejaculatory (but not non-ejaculatory) copulations occurring in the fertile phase. Additionally, we show that frequency of inspection of females by males and time spent in consortship were also highest during the fertile phase and that ejaculatory copulations and male pericopulatory behaviors were significantly correlated with levels of female sex hormones. Our findings indicate that the Barbary macaque shows a mating pattern during the cycle similar to that described for other members of the genus. More importantly, however, our study provides clear evidence that despite an extreme degree of promiscuity Barbary macaque males concentrate their reproductive effort to the fertile phase, implying that they are able to discern this period and that thus timing of ovulation is not concealed from them. Estrogen-related cues appear to be involved in the process of recognition of female reproductive status by males, but the exact nature of these cues and how male Barbary macaques use them remains to be clarified.     

Patterns of infant handling and relatedness in Barbary macaques (<Emphasis Type="Italic">Macaca sylvanus</Emphasis>) on Gibraltar

Among papionin primates, the Barbary macaque (Macaca sylvanus) shows the most extensive interactions between infants and group members other than the mother. Two different types of interactions occur: (1) long-lasting dyadic interactions between a handler and an infant, and (2) brief triadic interactions between two handlers involving an infant. Previous investigations showed that infant handling by males is best explained as use of infants to manage relationships with other males. In contrast, no adaptive explanation for infant handling by females emerged. Here, we compared the infant-handling pattern between subadult/adult males and subadult/adult females in a free-ranging group of 46 Barbary macaques on Gibraltar to test whether the relationship management hypothesis also applies to female handlers. We further investigated the infant-handling pattern of juveniles and used microsatellite markers to estimate relatedness between infant handlers and the infant’s mother. We found that males, females and juveniles all participated extensively in triadic interactions using infants of above-average related females. In contrast, only males and juveniles were highly involved in dyadic interactions with infants of related females, while females rarely handled infants other than their own. The pattern of infant handling was entirely compatible with the predictions of the relationship management hypothesis for males and mostly so for females. Moreover, our genetic analysis revealed that males and females differ in their partner choice: while females preferred to interact with related females, males had no significant preference to interact with related males. We further discuss the observed above-average relatedness values between infant handlers and the infant’s mother in the light of kin-selection theory.     

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.     

Molecular phylogeny of macaques: implications of nucleotide sequences from an 896-base pair region of mitochondrial DNA

We determined the nucleotide sequences of an 896-base pair region of mitochondrial DNA (mtDNA) from 20 primates representing 13 species of macaques, a baboon, and a patas. We compared these sequences and the homologous sequences from four macaques and a human against each other and deduced the phylogenetic relationships of macaques. The results from the phylogenetic analyses revealed five groups among the macaques: (1) Barbary macaque, (2) two species of Sulawesi macaques, (3) Japanese, rhesus, Taiwanese, crab-eating, and stump-tailed macaques, (4) toque, pig-tailed, and lion-tailed macaques, and (5) Assamese and bonnet macaques. The phylogenetic position of Tibetan macaque remains ambiguous as to whether it belongs to the fourth or fifth group. Phylogenetic trees revealed that Barbary macaque diverged first from the other Asian macaques. Subsequently, the four groups of Asian macaques diverged from one another in a relatively short period of time. Within each group, most of the species diverged in a relatively short period of time following the divergence of the groups. Assuming that the Asian macaques diverged from the outgroup Barbary macaque three million years ago (MYA), the divergence times among groups of Asian macaques were estimated at 2.1-2.5 MYA and within groups at 1.4- 2.2 MYA. The intraspecific nucleotide diversity observed among three rhesus macaques was so large that they did not form a monophyletic cluster in the phylogenetic trees. Instead, one of them formed a cluster with Japanese and Taiwanese macaques, whereas the other two formed a separate cluster. This implies that either polymorphisms of mtDNA sequences that existed before the divergence of these three species (ca. 700,000 years ago) have been retained in rhesus macaques or introgression has occurred among the three species.      

Social Relationships in Free-Ranging Male Macaca arctoides

Macaque social relationships differ greatly between species. Based on captive studies that focus mainly on females, researchers have classified stumptail macaque (Macaca arctoides) social relationships as tolerant, as indicated by a high rate of affiliation, frequent aggression, and symmetrical conflicts. To accumulate more data on male social relationships, which are relatively understudied, and to generate comparative data, we investigated male social relationships in a provisioned group of 68 free-ranging, naturally dispersing stumptail macaques in southern Thailand. We collected continuous focal animal and ad libitum data on 7 adult and 2 subadult males, recording social behavior during 283 contact hours between December 2006 and March 2007. Stumptail macaques of this population were less tolerant than predicted based on previous studies on captive groups: Rates of spatial proximity, affiliation, and aggression were low, most males directed affiliative behavior toward higher-ranking males, and conflicts were generally of low intensity and relatively asymmetrical. Thus, male stumptail macaques of the focal group appear to differ in their social style from a previous study of a captive group that mainly comprised of females. In some traits, they are even more intolerant than rhesus macaques, an intensively studied intolerant macaque species. We also compare our data on stumptail macaque males to those on other male macaques, but available data are too sparse to draw final conclusions.     

Male–Male Relationships in Lion-tailed Macaques (<Emphasis Type="Italic">Macaca silenus</Emphasis>) and Bonnet Macaques (<Emphasis Type="Italic">Macaca radiata</Emphasis>)

Socioecology suggests that female distribution in space is determined by the distribution of food resources and the male distribution is influenced by female distribution. Though studies have traditionally focused on females, males have received increasing attention in recent years. We compared male–male relationships in lion-tailed macaques and bonnet macaques. Because bonnet macaques have a high adult male:female sex ratio and are seasonal breeders whereas lion-tailed macaques have a low adult male:female sex ratio and are largely aseasonal breeders, we predicted that bonnet macaque males would be spatially and socially more tolerant of each other and would have less linear dominance relationships than lion-tailed macaques. We recorded male–male and male–female relationships in 1 group of wild macaques of each species via scan sampling and 1–0 sampling. The results revealed that lion-tailed macaque males largely remained at a distance from each other whereas bonnet macaque males remained in close proximity to one another. Lion-tailed macaque males were more agonistic toward each other whereas bonnet macaque males showed more affiliative interactions. The dominance hierarchy among lion-tailed macaque males was more linear than among bonnet macaque males. Our data support the hypothesis that the study of spatial structuring, temporality of interactions, and linearity of social relationships may contribute to a better understanding of macaque social systems.     

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.     

Reproductive success in relation to dominance rank in the absence of prime-age males in Barbary macaques

In some primate species dominance rank of males is correlated with reproductive success, whereas in other species this relationship is inconsistent. Barbary macaques (Macaca sylvanus) live in a promiscuous mating system in which males are ranked in a dominance hierarchy that influences their access to females. High-ranking males usually monopolize fertile females during their estrous period and show increased mating activities. Subadult males generally rank below adult males. For Barbary macaque females in the Gibraltar colony, there was no correlation between dominance status and reproductive success. Paternity data for 31 offspring collected over four consecutive breeding seasons were used to test whether male social rank was associated with reproductive success and whether reproductive success was mainly confined to a small number of males. Genetic variation was assessed using 14 microsatellite markers for a dataset of 127 individuals sampled in all five social groups of the Gibraltar colony. Paternity analysis was conducted for offspring in one social group only, where all in-group males were sampled. Eighty-three percent of the offspring could be assigned to an in-group candidate father; none of the extra-group males appeared to have sired an infant. Male dominance rank was not found to contribute to the observed variation in male reproductive output. Fifty-nine percent of the offspring was sired by two low-ranking males, whereas the two top-ranking males sired one-fifth. A highly significant correlation was found for male age and dominance rank. Reproductive success of subadult males might be explained by the gap in the age distribution of male group members. These missing prime males are usually regarded as serious competitors for older males. Subadult males may have gained easier access to females in their absence. In addition, the presence of inbreeding avoidance mechanisms, which might also have overpowered possible rank effects, cannot be excluded.     

Social Tolerance in Wild Female Crested Macaques (Macaca nigra) in Tangkoko‐Batuangus Nature Reserve,Sulawesi, Indonesia

In primates, females typically drive the evolution of the social system and present a wide diversity of social structures. To understand this diversity, it is necessary to document the consistency and/or flexibility of female social structures across and within species, contexts, and environments. Macaques (Macaca sp.) are an ideal taxon for such comparative study, showing both consistency and variation in their social relations. Their social styles, constituting robust sets of social traits, can be classified in four grades, from despotic to tolerant. However, tolerant species are still understudied, especially in the wild. To foster our understanding of tolerant societies and to assess the validity of the concept of social style, we studied female crested macaques, Macaca nigra, under entirely natural conditions. We assessed their degree of social tolerance by analyzing the frequency, intensity, and distribution of agonistic and affiliative behaviors, their dominance gradient, their bared‐teeth display, and their level of conciliatory tendency. We also analyzed previously undocumented behavioral patterns in grade 4 macaques: reaction upon approach and distribution of affiliative behavior across partners. We compared the observed patterns to data from other populations of grade 4 macaques and from species of other grades. Overall, female crested macaques expressed a tolerant social style, with low intensity, frequently bidirectional, and reconciled conflicts. Dominance asymmetry was moderate, associated with an affiliative bared‐teeth display. Females greatly tolerated one another in close proximity. The observed patterns matched the profile of other tolerant macaques and were outside the range of patterns of more despotic species. This study is the first comprehensive analysis of females’ social behavior in a tolerant macaque species under natural conditions and as such, contributes to a better understanding of macaque societies. It also highlights the relevance of the social style concept in the assessment of the degree of tolerance/despotism in social systems. Am. J. Primatol. 75:361‐375, 2013. © 2013 Wiley Periodicals, Inc.     

Is Diet Flexibility an Adaptive Life Trait for Relictual and Peri-Urban Populations of the Endangered Primate Macaca sylvanus?

Habitat loss, fragmentation and urban expansion may drive some species to marginal habitats while others succeed in exploiting urban areas. Species that show dietary flexibility are more able to take advantage of human activities to supplement their diet with anthropogenically abundant and accessible resources. The Barbary macaque (Macaca sylvanus) is an endangered species due to the loss of its habitat, and human pressure. The population of Gouraya National Park (Algeria) lives in a relictual habitat that constitutes about 0.6% of the species range. In addition, this population is a unique case where urban expansion favours contact zones between Barbary macaque habitats and a big city (Bejaia). We quantified the dietary composition of Gouraya macaques over an annual cycle with the objective to understand how diet flexibility of this species may help it adapt to a relictual habitat or cope with urban expansion. We recorded the phenology of plant species every month. This study shows that Gouraya macaques, compared to those living in other forest types of the distribution area, are under lower seasonal constraints. They consume a greater amount of fruit and seeds that are available throughout much of the year, and a lesser amount of costly to find and extract subterranean foods. Therefore the Gouraya relictual habitat appears as a favourable environment compared to other major habitats of that species. This study also shows that colonizing peri-urban zones increases the availability and species richness of diet resources for Barbary macaques as they consume more human foods and exotic plants than in farther sites. Adult males eat more human foods than adult females and immatures do. The exploitation of high-energy anthropogenic food could favour macaque population growth and expansion towards the city center associated with human/macaque conflicts. We recommend applying management actions to restore macaques back to their natural habitat.     

Outcast males and social structure among bonnet macaques (Macaca radiata)

Outcast males are a regular feature of rhesus (Macaca mulatta) and Japanese (M. fuscata) macaque societies but are rare among bonnet macaques (M. radiata). Apparently bonnets have other solutions than ostracism for their social problems. For example, in many troops the male-female ratio ranges from 0.7?1.0+; and, as the young adult males grow to full social and physical maturity, they remain in the troop and participate actively in social relationships. A few troops of bonnet macaques, however, have a network of social relationships which prevents the young males from being integrated into the social system; in some of these cases, male isolation occurs. A comparison of the social relations between males in bonnet macaque societies of both types suggests that societies with strong male-male bonds accommodate their growing males better than those with highly individual males.     

Male-infant relationships in semifree-ranging Barbary macaques (Macaca sylvanus) of affenberg salem/FRG: Testing the “male care” hypothesis

The infant-directed behavior of Barbary macaque males was analyzed in order to determine whether it is essential for an infant's survival during the first year and whether males interact selectively with closely related infants. Dyadic male-infant contacts were recorded in a large group of semifree-ranging Barbary macaques. Data collected during the first 12 weeks of life on each infant born in 1983 (n = 36) were analyzed. All adult and almost all subadult males established strong relationships with at least one infant. Almost two-thirds of the infants (22) had frequent contacts with one or several males. Males showed no preference for closely related infants. Sexual associations with an infant's mother during the preceding mating season had no significant effect. Natal males did not prefer infants of their own matrilineage. There was no evidence that contacts with males had a positive influence on infant survival or that other benefits to the infants resulted from these contacts. Instead, excessive carrying by males and females led to starvation of some very young infants and was a major cause of neonatal deaths in this population. Males interacted preferentially with infants that were born early in the birth season, had a high-ranking multiparous mother, and were male. Younger males established strong relationships with male infants only, while mother's rank was more important for older males. It is suggested that certain mothers prevented early contacts between their infants and males so that the observed preferences for certain infants were also a result of easier access to them. All results suggested that males interacted with infants for their own benefit.     

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.     

Interspecies pair housing of macaques in a research facility

The eighth edition of The Guide for the Care and Use of Laboratory Animals establishes social housing as the 'default' for social species including non-human primates. The advantages of social housing for primates have been well established, but small research facilities housing few primates in indoor cages have struggled with social housing as a result of limitations on appropriate housing and availability of compatible monkeys. Here, we report a novel approach to pair housing macaques - crossing species. We have successfully pair housed an intact male rhesus macaque with an intact male cynomolgus macaque, and an adult female rhesus macaque with numerous subadult female cynomolgus macaques. Monkeys in these pairs established dominant-subordinate relationships similar to same-species pairs. Rhesus and cynomolgus macaques can be successfully paired for the purpose of social housing in facilities with limited numbers of monkeys.     

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.     

The use of vocal signals in the social play of barbary macaques

Field studies in various species ofMacaca (Cercopithecidae) provided evidence for specific visual displays that typically accompany playful interactions. The aim of our study was to examine whether and when playing individuals would use auditory displays, i.e. vocalizations that often occur during social play as well. The study was conducted on a population of semi-free Barbary macaques (Macaca sylvanus) with a special focus on the composition and dynamics of playful wrestling (synonymous term: ‘rough-and-tumble play’). Analyses of dyadic encounters between subadult males allowed us to distinguish five types of playful behaviours and three types of vocalizations. The latter were clearly linked to encounters where effects of visual signals were impaired, e.g. during close body contact. During wrestling, vocalizations tended to increase in the beginning of an encounter, whereas the last seconds of wrestling often showed a decline in vocalization rate. Our results allowed us to conclude that these vocalizations may supplement or in many cases even substitute interactional effects of visual signals, e.g. the ‘play face.’     

Intra- and inter-group interactions of an all-male group of virunga mountain gorillas (Gorilla gorilla beringei)

Six unrelated male gorillas formed an all-male group within the Virunga mountain gorilla population. Frequent homosexual interactions characterized the high cohesiveness of this group. Such homosexual behavior reduced the inter-individual distances and increased the social tension between the two silverbacks in the group. The silverbacks retained “ownership” of the homosexual partners, but competed and fought with each other violently when the partners avoided or ignored their courtship. Neither submissive nor reassurance behavior was noted between the silverbacks. Thus, their relationships may not be explained in terms of dominance and subordinancy. However, the loser-support and mediating behavior observed in the group prevented them from engaging in severe fights. Aggression was always directed from the elder and dominant males to the younger and subordinate males, while supporting interactions occurred in the opposite direction. The blackbacks frequently supported the subadult aggressees by attacking the silverbacks, and the younger males displayed mediating behavior in violent fights between the silverbacks. The group's ranging was influenced by encounters with neighboring social units. The members avoided contact with other units and shifted their range after several encounters. On the other hand, when and after a subadult male had immigrated into their group, they frequently encountered other units and did not move away from the encounter site. An all-male group may not be a favorable unit for females to transfer to, but may be profitable for maturing males to associate with. Its formation is probably related to recent social change in the Virunga gorilla population.     

Social Behavior of Captive Indochinese and Insular Long-Tailed Macaques (Macaca fascicularis) Following Transfer to a New Facility

There are measurable differences in behavior, physiology, social organization, and geographic distribution within and between various species of macaques. We collected information on the social behavior of captive Macaca fascicularis from Indochina and island populations after they had been transferred to a new environment and new social groups. While some changes in behavior occurred over time, we found no decrease in high levels of agonistic behaviors. We interpret this finding in light of previous research reporting that long-tailed macaques show low levels of habitatuation to novelty and are highly aroused in comparison to other macaque species. We found predictable differences in behavior for males, females, and infants, in which infants played more, females had higher levels of contact proximity to other individuals, and males exhibited more sexual and threat behavior. A comparison of social behavior in long-tailed macaques from different origins indicate that Indochinese macaques are generally less affiliative and Indochinese males are more aggressive than their insular counterparts. Differences among macaque species, and within the fascicularis-group, should be considered in management of captive colonies and when interpreting research data.