The impact of paternity on male–infant association in a primate with low paternity certainty

In multimale groups where females mate promiscuously, male–infant associations have rarely been studied. However, recent studies have shown that males selectively support their offspring during agonistic conflicts with other juveniles and that father's presence accelerates offspring maturation. Furthermore, it was shown that males invest in unrelated infants to enhance future mating success with the infant's mother. Hence, infant care might provide fitness gain for males. Here, we investigate male–infant associations in rhesus macaques (Macaca mulatta), a primate with low paternity certainty as females mate with multiple partners and males ensure paternity less efficiently through mate‐guarding. We combined behavioural data with genetic paternity analyses of one cohort of the semi‐free‐ranging population of Cayo Santiago (Puerto Rico) and recorded affiliative and aggressive interactions between focal subjects and adult males from birth to sexual maturation (0–4 years) of focal subjects. Our results revealed that 9.6% of all interactions of focal subjects involved an adult male and 94% of all male–infant interactions were affiliative, indicating the rareness of male–infant aggression. Second and most interestingly, sires were more likely to affiliate with their offspring than nonsires with unrelated infants. This preference was independent of mother's proximity and emphasized during early infancy. Male–infant affiliation rose with infant age and was pronounced between adult males and male rather than female focal subjects. Overall, our results suggest that male–infant affiliation is also an important component in structuring primate societies and affiliation directed towards own offspring presumably represent low‐cost paternal care.     

Affiliative relationships between adult males and immature group members in naturally occurring ringtailed lemurs (Lemur catta)

Affiliative relations between adult males and immature group members were studied in three naturally occurring groups of ringtailed lemurs (Lemur catta) over a 12-month period at Beza-Mahafaly Reserve, southwestern Madagascar. No statistically significant difference was found in rates of affiliative interactions between adult males and older immatures (juveniles and adolescents) over reproductive seasons. However, some of the adult males in two focal groups increased their rates of affiliative behaviors with older immatures during the lactation and subsequent 1993 postmigration periods. Female involvement with infants during lactation season, the increasing independence of juveniles and adolescents, and length of male tenure may be factors contributing to such a pattern. Neither adult males nor immatures were significantly responsible for the initiation and maintenance of proximity in male-immature dyadic interactions. Neither dominance rank nor age-class of the adult male affected their rates of affiliative behavior with immatures. The majority of focal males exhibited an interest in infants and occasionally participated in alloparental care. It is suggested that adult males can benefit from affiliative relations with immatures in terms of opportunities for greater spatial centrality in the group, which can lead to enhanced predator protection and greater opportunities to develop affiliative relationships with females. Immatures can benefit from affiliation with males in relation to enhanced predator detection and protection, alloparental care, and opportunities to develop social skills. Am J Phys Anthropol 103:163–171, 1997. © 1997 Wiley-Liss, Inc.     

Male-female affiliative relationships in naturally occurring ringtailed lemurs (Lemur catta) at the Beza-Mahafaly Reserve,Madagascar

Affiliative behavior between adult male and female ringtailed lemurs was examined as part of a project concerning male affiliation with conspecifics of all age/sex classes. Males in three social groups were studied over a 12 month period. Male-female preferred partnerships existed, and were variable according to reproductive season. Dominance rank, age, or tenure of the male did not appear to affect either the number of partnerships or frequency of affiliative behaviors that males had with females. However, males residing in groups with fewer males exhibited both higher frequencies of affiliative interactions with females and were nearest neighbors to females more often than males living in a group containing more males. Females were found to be responsible for proximity maintenance of male-female dyads in the majority of cases. Neither reproductive season nor seasonal availability of food resources strongly affected the frequency of affiliative interactions between males and females, it is proposed that an important aspect of successful group membership for male ringtailed lemurs relates to the development of social relationships with adult females. Males can benefit from such relationships in terms of greater centrality to the spatial core of the group, which can result in enhanced predator protection, greater opportunities for social contact, and potentially greater access to estrous females. © 1996 Wiley-Liss, Inc.     

Intergroup affiliative interactions and intergroup transfer of young male Japanese macaques (Macaca fuscata)

The social interactions between young male Japanese macaques (Macaca fuscata) and members of two adjacent groups were studied. Young males usually associated with members of a single group. Although some young males occasionally interacted with members of the neighboring group, the frequency of their intergroup affiliative interactions was much lower than that of their intragroup interactions. The intergroup affiliative interactions were less symmetrical than the intragroup interactions. Three- or four-year-old males who remained in their natal group interacted with males of the neighboring group, whereas males over 5 years old did not. Young males revealed a dramatic change in their association partners from males in one group to those in another during the course of their intergroup transfer. Males who remained in their natal group did not attempt to interact with females of the neighboring group. In contrast, males who had transferred to a non-natal group interacted with females in their natal group. It is suggested that intergroup affiliative interactions and intergroup transfer of young male macaques are influenced by close associations between males. The immediate motivation for transfer of young natal macaques may be some attraction to males outside their group rather than sexual attraction to unfamiliar females.     

Absence of strongly kin-preferential behavior by adult female sooty mangabeys (Cercocebus atys)

The objective of this study was to test the hypothesis that kin-preferential behavior would be present in sooty mangabeys (Cercocebus atys), a species taxonomically close to baboons and macaques. The affiliative behavior of the adult female members of a large captive group of these mangabeys was analyzed to test this prediction. These females groomed, were approached by, were in proximity to, and were in contact with their kin significantly more than expected, but only when all kin were included in the analysis. Removal of only the mother-infant (less than 1 year) dyadic interactions removed all significant kin effects. Kin-preferential behavior was also absent in affiliative interactions among the adult females as a class. Affiliation between mothers and offspring significantly exceeded that for all other kinship categories (such as siblings, etc.), and affiliation with kin other than offspring did not differ from that with nonkin adults. In their interactions with nonkin, the adult females showed some preference (duration of grooming) for those adult females of similar age, an effect predicted by the intensity of interaction among members of the same age cohort during development. These similar-aged females may also be paternally related. In comparing these results with the existing literature on kin-preferential behavior, two conclusions may be reached: (1) age and degree of kinship are primary factors that must be considered in order to avoid the existing overgeneralization of the importance of kinship in primate social organization, and (2) the role and importance of affiliative behavior in kin-selection theory should perhaps be re-examined in light of questions raised by this study.     

Determinants of Affiliative Interactions between Adult Males and Lactating Females in Pigtail Macaques (Macaca nemestrina nemestrina)

In some species of Cercopithecine primates, unrelated adult males and females maintain affiliative relationships ('friendships') that are apparently unrelated to mating or parental care. This study investigated the occurrence of friendships in a captive group of pigtail macaques, and some of their possible determinants. Study subjects were six adult males and 15 adult females with their newborn infants. Females were focally observed for 2 h every week during the first 12 wk of lactation. With the exception of the fourth-ranking male, adult males showed little interest in initiating affiliative interactions with lactating females and their infants. Most episodes of contact and grooming were initiated by high-ranking females and directed to the alpha male. Because female grooming was not generally reciprocated by the alpha male, it is likely that females benefited from associating with him in terms of agonistic support or protection. Genetic data on paternity determination indicated that the fourth-ranking male, who displayed high levels of affiliation towards mother-infant dyads, sired most of the infants born in the group in the year prior to this study. Thus, whereas females may be interested in associating with males to obtain their support, some males may affiliate with females as a consequence of their previous mating relationships with them or to increase the chances of future mating success. Taken together, however, the findings of this study provide little evidence that adult males and lactating females maintain strong reciprocal bonds that may qualify as friendships.     

Greeting behavior during party encounters in captive chimpanzees

Party encounter situations were experimentally produced in a group of captive chimpanzees (Pan troglodytes verus) at the Primate Research Institute of Kyoto University, Japan. During weekends all subjects (two adult males and five adult females) usually stayed together in the rooms (Baseline condition). Under experimental conditions, we shut passages between rooms to divide the subjects into two groups. We examined the effects of temporal separation of group members on affiliative interactions, aggressive interactions, and simple proximity. The frequency of affiliative interactions between male and female chimpanzees and between female chimpanzees increased when they encountered one another after separation, irrespective of male identity or housing history. Therefore we considered affiliative interactions between males and females during party encounters as being the response between separated individuals. The same tendency was not found in the frequency of affiliative interactions between females or between males. Unlike affiliative interactions, neither aggressive interactions nor simple proximity were influenced by separation.     

Do Adult Male Spider Monkeys (Ateles geoffroyi) Preferentially Handle Male Infants?

Infant tolerance by adult males has been observed in many primate species with multimale–multifemale mating systems, but males do not usually initiate interactions with infants. In male philopatric species, such as spider monkeys, adult males within a community exhibit high levels of cooperation and affiliation, and they might therefore be motivated to create bonds with potential future allies. Based on this hypothesis we predicted that adult male spider monkeys would participate in infant handling more than adult females and they would preferentially direct handling toward male infants. Between January 2008 and July 2010, we collected 884?h of observation on a community of wild spider monkeys at Runaway Creek Nature Reserve in Belize. During this period we observed 120 incidences of affiliative interactions between infants and adults other than their mother. The adult initiated the majority of nonmother adult–infant interactions (78?%). All available infants (5 males, 7 females) were handled during the study. All 9 of the community adult males handled infants but only 7 of 14 adult females did so. Adult males handled infants significantly more often than did adult females and males also handled young infants more often than older infants. Significant infant sex differences in handling appeared in infants >6?mo when adult males handled males significantly more than females. The patterns of infant handling among age–sex class dyads reflect the affiliative social patterns that we see in adult spider monkeys. These results provide support for the hypothesis that adult males preferentially handle male infants as a strategy for fostering social bonds.     

The effects of temporary removal of the alpha male on the behavior of subordinate male vervet monkeys

The effects of temporary removal of the alpha male on the behavior of subordinate adult male vervet monkeys were evaluated. Twelve subordinate males from six captive multimale, multifemale vervet monkey groups were observed in two conditions: when all group members were present and when the alpha male was temporarily removed from each group. In the absence of the alpha male, subordinate males initiated more affiliative behavior and increased the amount of time spent in proximity to females but their rates of aggression were unaltered. Increased affiliative behavior was selectively directed to high-ranking females and their offspring. Under removal conditions, subordinate male behavior did not resemble that of alpha males in intact conditions: they differed in their proximity to and affiliative behavior towards other group members. In the absence of the alpha male, females increased their aggression towards subordinate males. These observations suggest that the presence of alpha males strongly inhibits subordinate males' behavior. When the constraints of the alpha male's presence are removed, subordinate males rapidly engage in behavior that may enhance their likelihood of attaining high rank. In combination with prior studies, the data also indicate that the behaviors involved in the maintenance of high rank by alpha males differ from those subordinates use to acquire dominance. Finally the current study supports the view that aggression by female vervets may be highly influential in determining male ascendency to dominant rank.     

Group unity of chimpanzees elucidated by comparison of sex differences in short-range interactions in Mahale Mountains National Park,Tanzania

Chimpanzees (Pan troglodytes) form multi-male and multi-female unit groups with fission–fusion grouping patterns. Short-range interaction (SRI) plays an important role in the unity of these groups and in maintaining social bonds among members. This study evaluated three models of chimpanzee social structure that differed according to the emphasis each placed on social bonds between the sexes, i.e., the male-only, the bisexual, and the male-bonded unit-group model. I investigated differences in SRI between the sexes among group members in well-habituated wild chimpanzees in Mahale Mountains National Park, Tanzania. I followed six focal adult males and six females, and quantified their respective SRI with other chimpanzees. Except between subordinate males and adult females, adults in general engaged in SRI with about 60–90% of the individuals with whom they made visual contact each day, whether in large or small parties. Although the number of social grooming (SGR) partners was limited, male–male SGR networks were wider than were either male–female or female–female SGR networks among adults. The number of contact-seeking behavior (CSB) partners was also limited, but dominant males had more CSB partners. Adult females mainly interacted by pant-grunt greeting (PGG) with adult males, but tended to do so mainly with the highest-ranking male(s) within visual contact. These results indicated that the social bonds among adult males were essential to group unity. Because of clear male dominance, adult females established peaceful coexistence with all group members despite less frequent SRI with subordinate males by maintaining affiliative social bonds with dominant males, thereby supporting the male-bonded unit-group model. Adult females had many female SRI partners, but these interactions did not involve performing conspicuous behaviors, suggesting that females maintain social bonds with other females in ways that differ from how such bonds are maintained with and between adult males.     

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.     

The development of affiliative and coercive reproductive tactics in male chimpanzees

Like many animals, adult male chimpanzees often compete for a limited number of mates. They fight other males as they strive for status that confers reproductive benefits and use aggression to coerce females to mate with them. Nevertheless, small-bodied, socially immature adolescent male chimpanzees, who cannot compete with older males for status nor intimidate females, father offspring. We investigated how they do so through a study of adolescent and young adult males at Ngogo in Kibale National Park, Uganda. Adolescent males mated with nulliparous females and reproduced primarily with these first-time mothers, who are not preferred as mating partners by older males. Two other factors, affiliation and aggression, also influenced mating success. Specifically, the strength of affiliative bonds that males formed with females and the amount of aggression males directed toward females predicted male mating success. The effect of male aggression toward females on mating success increased as males aged, especially when they directed it toward females with whom they shared affiliative bonds. These results mirror sexual coercion in humans, which occurs most often between males and females involved in close, affiliative relationships.     

The effects of infant births on male–female relationships in Cebus capucinus

Most primates are characterized by cohesive male–female bonds that are maintained year round. While recent studies have addressed the selective pressures influencing the evolution of male–female relationships in primates, we know relatively little about the proximate mechanisms affecting them. It has been demonstrated that newborn white‐faced capuchins (Cebus capucinus) attract the attention of other group members and this may be an important mechanism influencing male–female relationships. We studied two groups of C. capucinus in the Area de Conservación Guanacaste, Costa Rica, between February and July 2007. A total of 348 hr of focal data were collected on all adult males (n=6) residing in each of the study groups. During our study, 13 of the 14 group females were either pregnant or lactating, and 9 infants were born. We calculated an average daily affiliation rate between all group males combined and each adult female four weeks before and four weeks after the birth of her infant. Repeated measures ANOVAs revealed no significant changes in affiliation following infant births (F=2.262, df=1, P<0.176). Results remained nonsignificant for rank (F=1.550, df=1, P<0.260) and group membership (F=0.729, df=1, P<0.429). Infant sex was the only variable with a significant effect on affiliation rates between males and females (F=10.020, df=1, P<0.019). Adult males increased their affiliation with all adult females that gave birth to male infants (n=4), while their rates decreased with all but one of the adult females with female infants (n=4). While preliminary, these results indicate that the adult males may cultivate relationships with other males at a young age. Am. J. Primatol. 71:380–383, 2009. © 2009 Wiley‐Liss, Inc.     

Patterns of affiliation among immature rhesus monkeys (Macaca mulatta)

The affiliative interaction patterns of the immature members of a group of rhesus monkeys at the Yerkes Regional Primate Research Center reflected a strong bias toward matrilineal kin, although this effect was modified by age and sex variables. Association with kin decreased with age, particularly for males. Juvenile males showed less of a kin bias in their behavior than did juvenile females, especially for grooming. Juvenile males also exhibited a preference for interaction with other males. The diminished association with kin and the same-sex bias may be reinforced in adolescence as adult males begin to aggressively target adolescent males involved in agonistic encounters with females or immatures. Adolescent males did not decrease their levels of social interaction relative to those of adolescent females; however, these males preferentially associated with other males (predominantly their own age-sex class) and specifically avoided females and younger animals, both kin and nonkin. Avoidance may diminish conflicts with females or immatures which could result from association, thereby decreasing the potential for selective aggressive interference by adult males. Juvenile and adolescent females maintained strong ties with their kin and preferentially associated with other females and immatures. The breadth of interaction of females with other females may facilitate the establishment of dominance relationships as females mature. Familiarity and predictability may also decrease the necessity of more severe agonistic interaction.     

Adoption of a Wild orphaned ringtailed lemur infant by natal group members: Adaptive explanations

In December 1992 an infant ringtailed lemur, approximately 7 weeks of age, was orphaned in one of the regularly-censused social groups at the Beza-Mahafaly Reserve, southwestern Madagascar. The infant was initially adopted by a subadult (2 yr-old) male from the group. Continuous-time focal animal data were collected for a 12-hr period, from the time that the infant was retrieved by the young male, in order to document the adoption process. Ten members of the infant's social group (total group number=18) engaged in infant care behaviors over the 12-hr period. The subadult male spent the most time engaged in infant care, and he and one adult female exhibited the highest frequency of caregiving behaviors over the 12-hr period (p<0.001). Four adult males also initially cared for the infant. The orphan was one of only six infants in the reserve population to survive that year. She was censused two years later as an adolescent member of her natal group. Adaptive explanations for this adoption vary depending upon the care-giver. For the subadult male and adult female caregivers, kin selection can be suggested, as the infant was related to all females and immature animals in the group. Adult males may have exhibited caregiving behaviors as a strategy related to affiliation with adult females which could lead to potential mating and reproductive success.     

Paternity in Sooty Mangabeys

We determined paternity for 78 sooty mangabeys [(Cercocebus torquatus atys (Groves, 1978) equivalent to C. atys (Napier and Napier, 1967)], born between 1986 and 1993, using DNA profile analysis. The analysis is based on two independent assays of the genome of each individual via multilocus DNA probes. The mangabeys were members of either a large (n = 98) or a small (n = 18) group. Overall, during two periods of analysis in the large group, higher-ranking males sired more offspring than their lower-ranking counterparts did, though during one period the correlation between dominance rank and reproductive success is not significant. Of the two males in the small group, the alpha male sired all of the offspring during one period. There is a significant correlation between mounts and the number of surviving offspring each male sired in one birth year. Moreover, the same male did not always sire the offspring of a given female from year to year. Behavioral data focusing on male–offspring interactions show that offspring (n = 15) did not preferentially affiliate with their sire and that males affiliated with infants too infrequently for analysis. Thus, in a large sooty mangabey colony: (1) dominance rank generally predicts reproductive success; (2) adult males are not preferentially attracted to their offspring, or infants to their sires; and (3) the same male generally does not sire the offspring of a given female from year to year.     

Birth-season interactions of adult female Japanese Macaques(Macaca fuscata) without newborn infants

The affiliative interactions of 11 adult female Japanese macaques that did not deliver an infant during the 1981 birth season of the Arashiyama West troop were examined. Consideration was given to the effects of kinship as a structuring element in these birth-season interactions and to the degree of association with various categories of troop members based on age, sex, and (in the case of adult females) whether or not the females were new mothers. Females without infants interacted predominantly with their yearling off-spring, although it was the behavior of the offspring that precipitated the interaction. These females were active in soliciting affiliation with nonkin new mothers, whereas female matrilineal relatives with new infants approached and remained in proximity to them more than did nonrelated new mothers. Females without newborns groomed and approached nonkin infants more than infants within their own matriline, and these infants were predominantly those of females in the highest-ranking matriline of the troop. Adult males were responsible for 40% of all grooming received from nonkin by the females without newborns, and these males approached them significantly more than did other adult females without infants. These patterns demonstrate that the structure of social relationships is influenced by the particular dynamics of troop contexts such as birth seasons, as well as by enduring, broad-based affinities which are less affected by cyclic changes in troop context.     

Niche Divergence Among Sex and Age Classes in Black-and-White Snub-nosed Monkeys (Rhinopithecus bieti)

A wide range of dimorphic species exhibit intraspecific differences in feeding ecology and habitat use; however, studies comparing resource partitioning between males and females and between age groups occur mainly at the community and species level. We here classified the main habitat of black-and-white snub-nosed monkeys (Rhinopithecus bieti) –fir tree crown– into six microhabitats; examined the lichen-load of the microhabitats; and investigated the microhabitat use of age–sex groups within one-male units (OMUs: an adult male, several females, and juveniles) of R. bieti using instantaneous scanning sampling methods to test whether there is resource niche partitioning in social units of this sexually dimorphic primate in a reserve in Yunnan, China. Our results showed that adult females and juveniles often foraged in the outer layer of the fir tree crown, whereas adult males often foraged in the inner layer, closer to the trunk where food abundance was highest. Adult females and juveniles, however, both shifted microhabitat-use patterns to the inner layer of the fir tree crown when the adult male was absent from the tree. We suggested that the preference for and benefit of the central layer of fir tree crown lies in food availability, but that adult male competitively excluded group members. Microhabitat segregation may serve to maximize the fitness of the group members by reducing intragroup competition, while also increasing interindividual distance, thereby reducing the possible effects of scramble competition.     

Social behavior in fission–fusion groups of red uakari monkeys (Cacajao calvus ucayalii)

Primates living in large groups that divide to forage must have social systems compatible with this mode of living. Uakari monkeys (Cacajao spp.) live in large groups and exhibit a form of fission–fusion grouping, but their social organization is poorly understood. We present some of the first data on social behavior for this genus based on a study on Cacajao calvus ucayalii. They traveled in multimale multifemale groups of highly variable sizes, with bachelor units on the periphery. Adult males were affiliative, and adult females associated with more than one adult male. Adult females typically traveled with their dependent offspring and an older juvenile within the group. In parties of two or more males, individuals engaged in previously unreported display behaviors and acted together to aggressively chase other males. Breeding was seasonal, and mating occurred away from other group members. We speculate on the social organization of C. calvus ucayalii, in which dispersal may be bisexual and peripheral males are affiliative with one another. Affiliated males appear to cooperate in fighting and displaying to other males for access to females during the breeding season. Am. J. Primatol. 71:976–987, 2009. © 2009 Wiley‐Liss, Inc.     

Effects of reproductive and social variables on fecal glucocorticoid levels in a sample of adult male ring-tailed lemurs (Lemur catta) at the Beza Mahafaly Reserve, Madagascar

Glucocorticoids, a group of adrenal hormones, are secreted in response to stress. In male primates, variables such as breeding seasonality, dominance hierarchy stability, and aggressive and affiliative interactions can affect glucocorticoid levels. In this study, we examined interindividual differences in mean fecal glucocorticoid (fGC) levels among males in three groups of wild ring-tailed lemurs to better understand the physiological costs of group living for males in a female-dominant species that exhibits strict reproductive seasonality. Fecal and behavioral data samples were collected during one mating and two postmating seasons (2001 and 2003). The mean fGC levels were examined in relation to reproductive season, male rank, number of resident males, intermale and female-male agonism, and affiliative behavior with females. The mean fGC levels were not significantly elevated during mating season compared to the postmating period. During the mating season, male dominance hierarchies broke down and rank effects could not be tested; however, there was no relationship between male rank and fGC levels in the postmating periods. In 2001, males that resided in the group with the fewest males exhibited lower fGC levels during the postmating period. They also affiliated more with females than did males in the other groups. During the mating season of 2003, males engaged in more affiliative behaviors with females compared to the postmating season, but female-male agonism did not differ by season. However, rates of intermale agonism were significantly higher during mating compared to postmating periods, but such heightened agonism did not translate to a higher stress response. Thus, neither male-male competition for mates nor heightened agonism between males during the breeding season affected male fGC levels. Fewer males residing in a group, however, did have some effect on male-female affiliation and male fGC levels outside of the mating period. Males that live in a group with only a few (two or three) males may experience less physiological stress than those that live in groups with more males.