Significance of kin relations and individual preferences in the social behaviour of Cebus apella

Captive tufted capuchins (Cebus apella) formed a group characterized by greater affiliative behaviour within matrilines. Affiliation within the matriline is dependent upon social intimacy during infancy with matriline members. Courtship and mating are not identically distributed: subordinate and subadult males participate in a larger proportion of matings than of courtships. In all these aspects of social behaviour, variability across individuals contributes to the complex dynamics of the social group.     

Matrilineal overthrows in rhesus monkey groups

Between January 1976 and February 1983, there were four overthrows of the highest-ranking matriline in a group of rhesus monkeys. The overthrows were the result of members of multiple mainlines jointly attacking the adult female and adolescent members of the ranking matrilines. In three cases, the next-ranking matriline assumed highest position, while the surviving members of the deposed matrilines fell to the bottom of the hierarchy. Dominance relationships among other group members remained stable. High-ranking adult males vigorously defended the victims, but their efforts were ineffective. Unlike other members of the matrilines, adolescent males were not cohesive with their relatives during the overthrows and did not defend them. These young males were attacked by some adult and adolescent males. These incidents demonstrate the aggressive potential of females and underscore the importance of baboon and macaque females as the enduring and stable core of their social organization. The lack of effective participation by adult males demonstrates the independent functioning of this female core. These overthrows were similar in structure to incidents reported for other captive rhesus colonies and feral baboons, but no explanatory hypothesis posed accounts for all the data. Overthrows may be examples of opportunistic female behavior producing rapid changes in the normally stable female dominance system. Even if such events are rare, the deaths and reproductive failures within deposed matrilines may drastically affect inclusive fitness, counteracting the reproductive advantages of several years of dominance for a matriline.     

A study of correlates of hand preferences in squirrel monkeys (Saimiri sciureus)

The purpose of this study was to test the influence of sex, age, social rank, matriline membership, posture, and visual and tactual motor control on manual preferences inSaimiri sciureus. A well-established social group of 12 squirrel monkeys, aged 2 to 14 yrs and consisting of two matrilines with social rank known for each animal, was presented with four different food-reaching tasks and assessed for hand preferences with a minimum of 100 reaches per animal. Frequency of occurrence of hand preferences at the group level and degree of hand preferences at the individual level depended on posture and on whether the reaching act took place under visual or tactual guidance. Sex, age, social rank, and matriline membership were not found to determine frequency of occurrence, direction or degree of hand preferences with the exception of one task in which a significant negative correlation between the degree of hand preference and age was found. Nine out of 12 monkeys showed task-dependent changes in the hand they used preferentially while only three animals preferred the same hand in all four tasks. Significant preferences for the use of right or left hand on a given task were distributed almost equally between individuals. Thus, the results of this study suggest task-specific demands like posture and/or whether reaching was visually or tactually guided to be the major correlates of hand preferences in food-reaching tasks in squirrel monkeys.     

Induction of matrilineal rank instability by the alpha male in a group of Japanese macaques

Destabilizing alliances and ensuing rank changes occur infrequently in matrilineal dominance systems, and consequently very little is known about their dynamics. In one such type of alliance, called bridging, dominant individuals are ultimately responsible for subordinate monkeys out-ranking intermediate-ranking animals. Previously reported bridging alliances were based on sexual attraction, kinship ties, or special affinitive bonds between partners. In this paper we describe bridging alliances involving the alpha male in a group of Japanese macaques (Macaca fuscata) housed at the University of Montreal Laboratory of Behavioral Primatology. The comparison of rank relations in the presence and absence of the alpha male indicates that the latter was responsible for the destabilization of more than half of rank relations between members of the first and second matrilines. Another experiment revealed that the alpha male also induced extensive intermatriline reversals in priority of access to concentrated and highly prized food. These effects could be attributed to the male's consistent pattern of agonistic interventions in favor of the second matriline. However, the alpha male was not engaged in preferential affinitive relationships or reciprocally supportive interactions with the members of the second matriline. On the other hand, various lines of evidence indicate that the alpha male competed for dominance with the matriarch of the first matriline, suggesting that he might have consistently joined other individuals against that female and her kin in this context. The present data constitute further evidence for the nonaltruistic nature of aggressive interventions and the effectiveness of bridging alliances. © 1995 Wiley-Liss, Inc.     

Behavioural structuring of relatedness in the spotted hyena (Crocuta crocuta) suggests direct fitness benefits of clan-level cooperation

Spotted hyenas (Crocuta crocuta) are gregarious carnivores that live in multigenerational social groups, called clans, containing one to several matrilines. Members of multiple matrilines within a clan cooperate during dangerous interactions with inter- and intraspecific competitors. The evolution of cooperation may be influenced by relatedness between individuals, which in turn is influenced by reproductive skew and mate choice, dispersal and territorial behaviours. Behavioural data exist for spotted hyenas, but corresponding data on patterns of relatedness are unavailable; this lack of data makes it difficult to assess the relative importance of selection pressures favouring cooperative behaviour within and among groups. Therefore we conducted a longitudinal analysis of relatedness within a single large clan of spotted hyenas, as well as a cross-sectional analysis of relatedness among hyenas from multiple clans. Within a clan, patterns of relatedness reflected known pedigree relationships, and relatedness was higher within than among matrilines, even across generations. Although mean within-matriline relatedness varied among matrilines, it did not decline with matriline rank. On average, clan members were not related closely, due to high levels of male-mediated gene flow among clans, and relatedness declined very slightly across clan borders. Low mean relatedness within clans suggests that spotted hyenas cooperate with unrelated clan-mates against close paternal kin in other clans. Our data also suggest that spotted hyenas must derive large net direct fitness benefits from group living and cooperation.     

Complete separation along matrilines in a social spider metapopulation inferred from hypervariable mitochondrial DNA region

The distribution and quantity of genetic diversity may be profoundly influenced by the emergence and dynamics of social groups. Permanent social living in spiders has resulted in the subdivision of their populations in more or less isolated colony lineages that grow, proliferate and become extinct without mixing with one another. A newly discovered hypervariable mitochondrial DNA region allowed us to examine the fine scale metapopulation structure in the social Anelosimus eximius. We sampled 39 colonies in Ecuador and French Guiana and identified 25 haplotypes. The majority of colonies contained one haplotype. Additional haplotypes occurred in approximately 15% of the colonies, and were always closely related to the common colony haplotype. Our findings confirm that colonies consist of single matrilines, with within‐colony variation explained by mutations within the matriline. We thus found no evidence of mixing of matrilines. Likewise, colonies in a cluster often shared a haplotype, implying common colony ancestry. In few cases, however, haplotypes were shared between more distant colonies, providing evidence for occasional longer distance dispersal and/or widespread colony lineages. The geographical localities of colonies were incongruent with phylogenetic trees and haplotype networks, showing that some areas contained two or more matrilines. Hence, females do not migrate into foreign colonies, but faithfully remain within their own colony lineage, even when they disperse into new areas. These results indicate that the fine scale metapopulation structure of pure matrilines is maintained over the long term and that colony turnover is not extensive or radical enough to homogenize entire geographical areas. Genetic diversity is thus preserved to some extent at the metapopulation level.     

Family- and sex-specific vocal traditions in a cooperatively breeding songbird

Although songbirds provide well-known examples of cultural transmission of vocalizations, little is known about this process in species that live in stable social groups. Here I describe complex vocal traditions in a cooperatively breeding songbird, the stripe-backed wren (Campylorhynchus nuchalis). Repertoires of stereotyped calls were recorded from individually marked males and females in cooperative family groups. Males in the same patriline, whether in the same group or in different groups, had call repertoires that were nearly identical. Females in the same matriline also had identical call repertoires; however, female calls never matched the calls of males in the same group or in any nearby groups. Unrelated birds almost never shared calls. Call repertoires are apparently learned preferentially from same-sex relatives within family groups, so that call traditions separately follow patrilines and matrilines. This unique pattern of transmission results in vocal cues that reflect both sex and kinship.     

Mate choice by lineage in three captive groups of rhesus macaques (Macaca mulatta)

The hypothesis that the matrilineal affiliation of 410 infants born in three captive groups of rhesus macaques is independent of the patrilineal affiliation of these infants was tested. Preferential mating with particular patrilines was observed for matrilineal members. We conclude that lineage affiliation does influence mate choice of rhesus macaques, at least when a large number of matrilines and relatively few patrilines which include natal males are represented in the group. Such nonrandom mating might explain high levels of genetic heterogeneity reported among matrilines within rhesus groups, despite high rates of male emigration, and is consistent with the maintenance of high levels of within-matriline kinship which might promote cooperative behavior among matriline members.     

Social diffusion of novel foraging methods in brown capuchin monkeys (Cebus apella)

It has been reported that wild capuchin monkeys exhibit several group-specific behavioural traditions. By contrast, experiments have found little evidence for the social learning assumed necessary to support such traditions. The present study used a diffusion chain paradigm to investigate whether a novel foraging task could be observationally learned by capuchins (Cebus apella) and then transmitted along a chain of individuals. We used a two-action paradigm to control for independent learning. Either of two methods (lift or slide) could be used to open the door of a foraging apparatus to retrieve food. Two chains were tested (N1=4; N2=5), each beginning with an experimenter-trained model who demonstrated to a partner its group-specific method for opening the foraging apparatus. After the demonstration, if the observer was able to open the apparatus 20 times by either method, then it became the demonstrator for a new subject, thus simulating the spread of a foraging tradition among 'generations' of group members. Each method was transmitted along these respective chains with high fidelity, echoing similar results presently available only for chimpanzees and children. These results provide the first clear evidence for faithful diffusion of alternative foraging methods in monkeys, consistent with claims for capuchin traditions in the wild.     

The influence of social affiliation on individual vocal signatures of northern resident killer whales (Orcinus orca)

Northern resident killer whales (Orcinus orca) live in highly stable groups and use group-specific vocal signals, but individual variation in calls has not been described previously. A towed beam-forming array was used to ascribe stereotyped pulsed calls with two independently modulated frequency contours to visually identified individual killer whales in Johnstone Strait, British Columbia. Overall, call similarity determined using neural networks differed significantly between different affiliation levels for both frequency components of all the call types analysed. This method distinguished calls from individuals within the same matriline better than different calls produced by a single individual and better than by chance. The calls of individuals from different matrilines were more distinctive than those within the same matriline, confirming previous studies based on group recordings. These results show that frequency contours of stereotyped calls differ among the individuals that are constantly associated with each other and use group-specific vocalizations, though across-group differences were substantially more pronounced.     

Prevalence of muzzle-rubbing and hand-rubbing behavior in wild chimpanzees in Mahale Mountains National Park, Tanzania

In 1998, four chimpanzees in the Mahale Mountains National Park, Tanzania, were observed wiping their mouths with non-detached leaves or stalks of grass, or rubbing their mouths with a tree trunk or branch, especially while eating lemons. The number of mouth-wiping/rubbing individuals increased to 18 in 1999. By 2005, 29 chimpanzees were documented wiping/rubbing their muzzles in this way. Although it is difficult to determine whether the chimpanzees acquired this behavior as a result of trial and error or social learning, the fact that chimpanzees at other sites perform this behavior with detached leaves or leafy twigs much more often than with intact items suggests the possibility that cleaning with intact plant parts at Mahale spread via social learning.     

The effects of fur rubbing on the social behavior of tufted capuchin monkeys

Fur rubbing has often been attributed as a social as well as a medicinal function in capuchin monkeys, yet to date there have been no studies investigating the effects of fur rubbing on subsequent group dynamics. Here, we report for the first time how social group cohesion is affected by fur rubbing in tufted capuchin monkeys. Fifteen captive capuchins were each observed six times for 45 min, three times following the provision of materials typically used for fur rubbing (onion) and three times following control food items (apple). When compared with the apple condition, monkeys significantly increased proximity to one another in the first 15 min of the onion condition, which is when most fur rubbing took place. Moreover, monkeys were more likely to spend time in groups when fur rubbing but less likely to spend time in groups when manipulating the onion in other ways. In subsequent periods monkeys were less likely to be in proximity to one another in the onion condition compared with the apple condition. Aggression between group members was elevated whereas affiliation was decreased throughout the onion condition. In short, capuchins spent more time further apart and engaged in more aggressive acts and shorter affiliative acts following fur-rubbing bouts. It is possible that these differences in behavior could be owing to differences in how the monkeys competed for and interacted with the items presented in each condition rather than due to fur rubbing as such. Alternatively, fur rubbing with pungent materials might interfere with olfactory cues used to regulate social interactions within a group and thereby cause increased levels of aggression.     

Matriline effects on metamorphic traits in a natural system in the European common frog (Rana temporaria)

Successful reproduction is an important determinant of the fitness of an individual and of the dynamics of populations. Offspring of the European common frog (Rana temporaria) exhibit a high degree of variability in metamorphic traits. However, environmental factors alone cannot explain this phenotypic variability, and the influence of genetic factors remains to be determined. Here, we tested whether the maternal genotype influences developmental time, body size, and body condition of offspring in a forest pond in Germany. We collected fertilized eggs from all 57 clutches deposited in the pond. We used multilocus genotypes based on seven microsatellite loci to assign metamorphosed offspring to mothers and to determine the number of fathers for a single matriline. We tested the influence of genetic effects in the same environment by comparing variability of metamorphic traits within and between full‐sib offspring grouped to matrilines and tested whether multiple paternity increases the variability of metamorphic traits in a single matriline. The variability in size and body condition was higher within matrilines than between them, which indicates that these traits are more strongly influenced by environmental effects, which are counteracting underlying genetic effects. The developmental time varied considerably between matrilines and variability increased with the effective number of fathers, suggesting an additive genetic effect of multiple paternity. Our results show that metamorphic traits are shaped by environmental as well as genetic effects.     

Evidence of social learning in black-and-white ruffed lemurs (Varecia variegata)

Although many studies have examined social learning capabilities in apes and monkeys, experiments involving prosimians remain largely absent. We investigated the potential for social learning in black-and-white ruffed lemurs using a two-action foraging task. Eight individuals were divided into two experimental groups and exposed to conspecifics using one of two techniques to access food. Subjects were then given access to the apparatus and their retrieval techniques were recorded and compared. All subjects made their first retrieval using the technique they observed being demonstrated, and there were significant differences between the two groups in their overall response patterns. These results suggest that prosimians are capable of social learning and that additional long-term field studies may reveal the presence of behavioural traditions similar to those found in other primates.     

Dominance competition through affiliation and support in Japanese macaques: An experimental study

It has been proposed that monkeys direct grooming to high-ranking individuals in an attempt to obtain agonistic support in return. But whether these two categories of interactions are causally related has proven difficult to establish. Part of the problem stems from the fact that in stable groups social relationships reflect an equilibrium state and that behaviors need only be performed at low rates and long intervals to maintain the current social structure. In theory, however, if affiliative and supportive interactions are indeed causally related, it should be possible to accentuate their temporal relation, hence their causal dynamics. For example, destabilizing dominance relations can be expected to induce competition for status and force individuals to deploy behavioral tactics for settling new rank relations. We experimentally induced rank reversals in a captive group of Japanese macaques (Macaca fuscata) composed of three matrilines (A-B-C rank order). A reversed C-A-B order composed of three individuals per matriline was maintained for 2 weeks. The results show the close temporal relation among (i) asserting one’s rank, (ii) competing for access to dominants through affiliation and interferences in affiliation, (iii) receiving support from dominants against lower-ranking individuals, and (iv) supporting dominants against subordinates. These findings are compatible with one version of the affiliation-for-support hypothesis, namely that monkeys affiliate with dominants as a way to assert their position in the hierarchy. In a functional perspective, mutual selfishness provides a better explanation than reciprocal altruism because the possibility that both groomers and supporters derive immediate net benefits cannot be excluded.     

Sex differences in infant integration in a semifree-ranging group of Barbary macaques (Macaca sylvanus,L. 1758) at Salem,Germany

Sixteen multiparous Barbary macaque females with newborns were studied over a 16 month period within the context of their naturally formed group. Analysis of their social behavior revealed 1) triadic interactions involving focal females, their newborns, and other group members occurred mainly with other females; and 2) mothers with female newborns interacted mainly with females of their own matriline, while mothers with male newborns interacted mainly with nonmatriline females. Observed in two successive birth seasons, this pattern indicates that partners of maternal interactions chose each other according to the sex of the newborn. Measures of distance from the mother also reflected differences between infants of different sex. At about five months of age, female infants were observed close to their mothers significantly more often than males. This finding follows the pattern of a sex-specific infant socialization process which integrates female infants into the network of their matrilines and male infants into the broader group. This sex-specific integration pattern is interpreted as supporting female philopatry and male dispersal. © 1995 Wiley-Liss, Inc.     

Social after-effects of fur rubbing in tufted capuchin monkeys (Cebus apella): increased antagonism and reduced affiliation

Fur rubbing is widely believed to have a social bonding function in capuchin monkeys, yet a recent study of tufted capuchins revealed increased levels of aggression and reduced levels of affiliation after fur-rubbing bouts. This observed decrease in group cohesion may be attributable to increased intragroup competition for fur-rub material rather than being a direct effect of fur rubbing itself. To test this hypothesis, we separated individual tufted monkeys (Cebus apella) from their social group and provided them with fur-rub material or control material, thereby avoiding intragroup competition. After engagement with materials, we released subjects back into their social group and observed their subsequent interactions with group members. We found that subjects were more likely to encounter aggression and less likely to receive affiliation from others in the fur-rub condition than in the control condition. These results support the idea that fur rubbing carries social after-effects for capuchin monkeys. The precise mechanisms of the observed effects remain to be clarified in future studies.     

Osteon remodeling dynamics in the Cayo Santiago Macaca mulatta: The effect of matriline

At the microstructural level, bones remodel throughout life. This process is recorded in bone cortex as osteons. A more comprehensive understanding of the interaction between genetic regulation and environmental factors in osteon remodeling will increase the value of this skeletal record and enable more accurate reconstruction of individual life histories. The purpose of this study was to examine the contribution of maternal lineage to normal age and sex variation in osteon remodeling dynamics in Macaca mulatta. Femoral cross sections from 57 Cayo Santiago-derived rhesus macaques representing five matrilines were examined to evaluate the effect of genetic relatedness on osteon remodeling dynamics. Analysis of variance revealed an effect of maternal lineage on osteon area and Haversian canal area. The other variables did not differ significantly among matrilines. Analysis of covariance revealed no significant interactions among age, sex, and matriline for any of the microstructural variables.     

Secondary sex ratio variation in the Cayo Santiago macaque population

Secondary sex ratios (SSR) were calculated from 1,385 offspring delivered by 372 females in the Cayo Santiago population of free-ranging rhesus monkeys (Macaca mulatta) from 1976 through 1984. The SSR for the entire colony ranged from 0.86 to 1.46 males per female (combined total: 1.08), but no significant difference was observed (P > .05). SSR values were compared among the troops for each year. The SSR differed significantly among the six social groups (P < .05) only in 1978. The annual SSR of each troop was compared over 9 years. Significant variation was found only in group O. The annual SSR was significantly skewed (P < .05, males > females) for three troops in 3 separate years. The SSR did not vary according to troop rank. No significant difference was found among the 17 matrilines of the population, but comparison of matrilines within each social group revealed a significant difference in the SSR (P < .02) for the three matrilines in group I. This was due to the significantly skewed SSR (P = .0080, females > males) of the DM genealogy in that troop. SSR values were not related to matrilineal rank. Individual dominance rank did not bias the SSR. Complete reproductive histories for 266 females showed no evidence of significantly skewed SSR values. Age-related effects on the SSR were examined by using cross-sectional and cohort-based analyses. The SSR did not vary significantly (P > .05) with maternal age, but it was significantly skewed (P < .05) toward males at the ages of 5 and 9 years. Parity had no significant effect (P > .05) on SSR values. Wide variation occurred in the SSR of the Cayo Santiago population. Rank-related adjustment of the SSR at the level of the troop, matriline, or individual, as reported in short-term studies of other primate social groups, may reflect normal annual variation in the SSR evident only from longitudinal observations of large multigroup primate populations.     

Contexts of rubbing behavior in Alouatta guariba clamitans: a scent‐marking role?

Rubbing behaviors are well known in several primate species and are usually seen as scent-marking behaviors, with several functions proposed but still widely debated. The genus Alouatta is highly sexually dimorphic and a suitable subject for the study of sexual and hierarchical divergences associated with rubbing behavior: males should mark more than females, and dominant individuals more than subordinate ones. Three wild groups of Southern brown howler monkeys, Alouatta guariba clamitans, were studied at Morro Geisler, Indaial, Brazil, from September 2004 to February 2005. One hundred and twenty-three rubbing episodes were registered; data on performers and associated contexts showed that anogenital, dorsum and hyoid regions were the most often rubbed. Adult males rubbed significantly above expected levels, whereas subordinated females and juveniles tended to rub below the expected levels. Females were the main performers of anogenital rubbing, often preceded by defecation. The predominance of rubbing in males probably serves an important function in intrasexual communication and social interactions. Intrasexual competition can also lead to a relationship between rubbing and social status in females. Hyoid and sternum rubbing by males are probably agonistic signals associated with extragroup conflict. The possible cleaning function of anogenital rubbing does not preclude a communicative function. Whether rubbing behavior in howlers is solely for the function of scent marking or can also be a visual signal (e.g. as a display or to color the substrate with pigment) requires further study.