Third-Party Ranks Knowledge in Wild Vervet Monkeys (Chlorocebus aethiops pygerythrus)

The Machiavellian/Social Intelligence Hypothesis proposes that a complex social environment selected for advanced cognitive abilities in vertebrates. In primates it has been proposed that sophisticated social strategies like obtaining suitable coalition partners are an important component of social intelligence. Knowing the rank relationships between group members is a basic requirement for the efficient use of coalitions and the anticipation of counter-coalitions. Experimental evidence for such knowledge currently exists in only few species. Here, we conducted rank reversal playback experiments on adult females belonging to three different groups of free-ranging vervet monkeys (Chlorocebus aethiops pygerythrus) to test their knowledge of the female hierarchy. Playbacks simulating rank reversals (subordinate aggressing a dominant) induced longer looking times than playbacks simulating a dominant aggressing a subordinate. Vervet monkey females therefore seem to compute the rank relationships between other females. Our results suggest that detailed social knowledge about rank relationships may be widespread in primates and potentially also in other species living in stable groups.     

Sociometrics of Macaca mulatta: II. Decoupling centrality and dominance in rhesus monkey social networks

The concept of the linear dominance hierarchy and a much less precise notion of a central/peripheral ordering of individuals have been prominent among the ideas about social organization of monkey groups. Although the latter has seldom been quantified, the ranks of individuals in the two orders are usually assumed to be correlated. This paper reports on a longitudinal study of a free-ranging group of rhesus monkeys. The individual histories of progression of dominance rank and an independently determined measure of centrality in the social grooming network are compared among a set of males. Centrality is not a static correlate of dominance rank as implied by the findings of short-term studies. Rather, centrality is a more sensitive indicator of status than is dominance rank, to which it is related in a dynamic fashion. Small changes in dominance rank may be followed by large changes in centrality. An increase in centrality may facilitate rise in dominance rank. These findings suggest a complex psychology of status, rather than a simple causative relation between the two variables.     

A case report of a male rank reversal in a group of wild white-faced capuchins (Cebus capucinus)

During the course of a study of social relationships in wild, white-faced capuchins at Lomas Barbudal, Costa Rice (May 1990–May 1993), the alpha male was deposed by a subordinate male. The rank reversal was preceded by a decline in proximity maintenance by females to the alpha male, and an increase, in the amount of aggression directed toward the alpha male by the beta female and her female coalition partners. At the time of the rank reversal, females switched from giving thegargle vocalization exclusively to the old alpha male to gargling to the new alpha male; however, juveniles were less consistent with regard to which male they gargled to. At the time of the rank reversal, most adult females reduced the time spent in proximity and grooming with the old alpha male, and increased the time spent in proximity and grooming with the new alpha male. In contrast, juveniles' patterns of affiliation with males did not change in a predictable way following the reversal. The social strategies employed by capuchin monkeys during this rank reversal are compared with those of chimpanzees.     

Estrous behavior of free-ranging rhesus monkeys (Macaca mulatta)

The sexual behavior of a group of free-ranging rhesus monkeys (Macaca mulatta) was studied for 13 consecutive months in an attempt to determine whether or not sexual activity occurred year-round, and the importance of sexual attraction to rhesus monkey social organization.Estrous behavior was seen both inter-menstrually and peri-menstrually, producing a shorter mean estrous cycle length than reported by other workers. New data was gathered on the interrelationships among age, dominance rank, and sexual activity; son-mother and brothersister matings; and sexual favoritism among free-ranging rhesus monkeys.A few females who failed to conceive during the fall breeding season showed cyclic estrous behavior throughout the entire annual cycle. Hypotheses are given as to possible physiological bases for birth season sexual cycles.Several forms of inter-animal bonding, including sexual bonding, are enumerated, and their importance to rhesus monkey social organization discussed.     

Male rank,reproductive behavior,and reproductive success in free-ranging rhesus macaques

Paternity assessment through DNA fingerprinting by synthetic oligonucleotide probes was applied to one birth cohort in a social group of free-ranging rhesus macaques (Macaca mulatta) on Cayo Santiago. The 11 group males and 9 males from other groups were observed mating with the females. Paternity was determined for 11 of the 15 infants. Male dominance rank was not associated with reproductive success. High-ranking resident males (N=5) sired 27% of the infants born during a one-year study. Four of the 11 infants of known paternity were sired by males of other social groups. The four infants of unknown paternity were sired either by males not observed mating with the females or the low-ranking male who was not fingerprinted. Male dominance rank was not associated with reproductive activity during conception cycles. These results suggest that the effect of rank on male reproductive success is not a predictable correlation, but a conditional probability.     

Social Relationships Among Ring-Tailed Lemurs (Lemur catta) in Two Free-Ranging Troops at Berenty Reserve, Madagascar

We observed two free-ranging troops of ring-tailed lemurs at the Berenty Reserve, Madagascar. Kinship affinities in these troops are known only for mothers and their offspring 4 years of age. We attempted to quantify social relationships. Almost all agonistic interactions were dyadic, and triadic agonistic interactions, such as alliances, were very rare. Dominance hierarchies in both sexes in the two troops were not linear. As in cercopithecine monkeys, mothers were dominant over their adult daughters. However, the daughters were not ranked immediately below their mothers. Close proximity and social grooming occurred more frequently between closely related females, such as mother–daughter and sister–sister dyads, than between unrelated females. Frequent-proximity relations also occurred between adult males that had emigrated from another troop and entered the present troop together, even though they did not rank closely to one another. Subordinates were likely to groom and to greet dominants more frequently than vice versa. During group encounters, particular females were involved in agonistic interactions with animals of other troops, regardless of dominance rank. Adult males, regardless of their dominance rank, but not adult females, constantly tried to drive solitary males away.     

Geophagy as a therapeutic mediator of endoparasitism in a free-ranging group of rhesus macaques (Macaca mulatta)

Parasite levels were determined for 141 members of a naturally formed social group of rhesus macaques living under free-ranging conditions. Results indicate that group members harbor Trichuris trichiura, Balantidium coli, and large numbers of Strongyloides fuelleborni. Parasite counts decrease significantly with age in this population. Females have significantly fewer parasites than males and a significantly lower prevalence of multiple infections. There were no rank effects regarding parasitosis. While 89% of the animals examined are infected with one or more species of enteric parasite, the prevalence of diarrhea is negligible (2%). The low prevalence of diarrhea in the presence of high parasite loads may be due to the practice of geophagy, which is engaged in by 76% of group members. Soil eaten by these monkeys contains large amounts of kaolinitic clays. Kaolin-based pharmaceuticals (i.e. Kaopectate^®) are commonly used in human populations to treat diarrhea and intestinal upsets. The mechanical and pharmaceutical properties of the natural kaolinite-based clays may counteract the effects of parasitosis in this free-ranging population. Am. J. Primatol. 44:71-82, 1998. © 1998 Wiley-Liss, Inc.     

Male and Female Reproductive Success in <Emphasis Type="Italic">Macaca sylvanus</Emphasis> in Gibraltar: No Evidence for Rank Dependence

The relationship between social rank and reproductive success is one of the key questions for understanding differences in primate social group structures. We determined the paternity of 18 infants in a social group of Barbary macaques (Macaca sylvanus) born over a period of 6 yr in the provisioned, free-ranging colony in Gibraltar. We successfully used 13 pairs of primers of variable microsatellite loci to amplify DNA from blood and hair samples and applied the computer programs CERVUS 2.0 and KINSHIP 1.3 to assign paternity to 13 candidate males. We collected data for 19 females that had given birth to 66 infants over a period of 7 yr. We used paternity analyses and female birth records to test the hypothesis that social rank is correlated with reproductive success. Results showed that numbers of paternities and maternities were equally distributed among all reproducing individuals in the social group regardless of rank. Subadult males reproduced as often as adult males. High-ranking females did not start to reproduce earlier than low-ranking females. Interestingly, there was a tendency toward a positive correlation between the ranks of mothers and the ranks of the corresponding fathers. It might be concluded either that a correlation between social rank and reproductive success is generally absent in Barbary macaques or that artificially favorable environmental conditions in Gibraltar preclude any correlation between social rank and reproductive success.     

Playmate relationships of immature free-ranging Japanese monkeys at Katsuyama

The playmate relationships of immature Japanese monkeys were analyzed with respect to age, sex, and dominance rank class of the matrilines in a larger-sized free-ranging group. One-year-old immature males showed the largest number of play partners and the highest frequency of social play. Older immature females tended to play with younger animals of both sexes, whereas immature males of all ages played with same-sexed and like-aged peers. While high-ranking immature males continued their play partnerships with other animals until 4 years of age, middle/low-ranking males did not. The large number of peers and possible play partners may intensify their selectivity of play partners in relation to dominance. The forming of playmate networks by high-ranking immature males may explain the delay in group shifting of high-ranking animals.     

Patterns of fight interference in free-ranging rhesus monkeys

Rhesus monkeys occasionally break up fights among conspecifics and this phenomenon may be called “interference.” The present study describes the patterns of interference in a group of free-ranging rhesus monkeys and evaluates the effect of this behavior onMacaca mulatta social organization. Data were collected at Cayo Santiago. Strong sexual differences were found in the patterning of interference behavior. Females tended to help victims of aggression and animals from the interferer's own genealogy, especially juveniles. In addition, females were likely to interfere as subordinate to the target animal. Natal and non-natal males oriented toward unrelated adult females and generally only interfered in fights if dominant to the target animal. Further, the males helped victims of aggression significantly less often than females did. Contrary to expectation, the dominant males were noteworthy neither for the quantity nor the effect of their interference. In general, the findings reinforce the notion that females are the stable and central part of a rhesus monkey social group. The findings also suggest that interference plays a role in the maintenance of group stability and cohesion.     

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.     

Sociological study on the troop fission of wild

During the period from June to July 1983, the Hanyama-A troop of wild non-provisioned Japanese monkeys on Yakushima Island began to show signs of troop fission. Adult females together with their infants and juveniles subdivided into two groups, the Hanyama-K group and Hanyama-M group. After the subdivision, all of the troop males were observed vacillating between these two female groups. During the mating season, non-troop males were also observed moving around the two female groups. After this mating season, one of these non-troop males was found to have entered and become the alpha male in one of the groups, while higher-ranking adult males of the original troop settled into the other group. Each fissioned group was strongly considered to be composed of either high-ranking matrilines or low-ranking matrilines as observed previously in provisioned troops. The dominance relation between the two fissioned groups indicated that dominance rank reversal between these two female kin groups must have occurred during the course of subdivision of the troop. However, different from most previous cases of troop fission, there was no indication that males ever participated in the subdivision of the original female group. This was disrupted not as a result of males' involvement, but only as a result of antagonism among females, which initiated the troop fission. The main factor which appeared to determine when and in which fission group males eventually settled was the competition between the troop males' coalition and non-troop males and their ability to monopolize females. The present process of troop fission suggests a dual strategy between males and females (Wrangham, 1979, 1980) even in the society of Japanese macaques.     

Factors affecting social behavior and reproductive success of male rhesus monkeys

This paper reviews aspects of life history that influence the reproductive success of male rhesus monkeys. Recent theories propose that there is some optimum level of inbreeding for each population and that behaviors related to group transfer by males are the result of selection pressure toward such an optimum. Group changing by males is clearly linked to the effects of testosterone at sexual maturation. A male’s maternal genealogical rank is not consistently related to the age at which it leaves the natal group, but social interactions within the natal group may influence the age of departure. Choice of the new group is influenced by the operational sex ratio and the presence of maternal relatives. Rank in the new group is positively correlated with seniority. Seniority, in turn, is influenced by the rank of the male’s natal group, his mother’s genealogical rank, and the presence of male siblings in the new group. Much of this effect is due to the high mortality of males born to females and/or groups of low rank. Most studies show a positive association between male reproductive success and rank. Males from high-ranking groups and/or maternal genealogies that join groups containing brothers tend to remain in those groups longer, attain a higher rank, and probably achieve higher levels of reproduction than other males.     

Social and environmental factors affecting fecal glucocorticoids in wild, female white-faced capuchins (Cebus capucinus)

Assessing glucocorticoid levels in free-ranging nonhuman primates provides a means to determine the social and environmental stress load for individuals. We investigated the effect of four proximate variables--reproductive state, season, male rank stability, and dominance rank--on the level of fecal glucocorticoids (cortisol metabolites) in eight adult female white-faced capuchin monkeys in Costa Rica. Reproductive state, season, and male rank stability significantly affected fecal glucocorticoids while female dominance rank did not. Cortisol levels were significantly higher in pregnant females as compared with lactating or other reproductive states. Cortisol levels were higher among females during the dry season compared with the wet season, suggesting a metabolic adaptation to maintain homeostasis in drier, hotter conditions. Although unfamiliar males present a greater infanticidal threat than do familiar ones, we found that females experienced higher glucocorticoid levels during male rank instability events, regardless of whether the alpha male role was taken over by a familiar or an unfamiliar male. Our findings provide important benchmark and comparative data for future studies on the variables that affect glucocorticoid levels in this species and other mammals.     

Female-female social relationships in wild white-faced capuchin monkeys,Cebus capucinus

A single social group of wild white-faced capuchin monkeys was studied for a period of 26 months at Lomas Barbudal Biological Reserve, Costa Rica. A total of 604 hr of focal animal data was collected on six adult females in a group of 21 monkeys. Females could be ranked in a stable, linear dominance hierarchy. Adult females spent much more time in proximity to other adult females than to adult males. Females groomed other females twice as often as they groomed males, and about 55 times more often than males groomed males. Females tended to groom up the dominance hierarchy, and dyads with smaller rank distances groomed more often. Higher-ranking females nursed infants other than their own at lower rates than did lower-ranking females; however, females nursed infants of females ranked both above and below them. Although lower-ranking females were more likely than higher-ranking females to be the victims of aggression, higher-ranking females were not necessarily more aggressive than lower-ranking females. In 96% of female-female coalitions vs. a female, the victim was lower-ranking than both coalition partners; in the remaining 4%, the victim was intermediate in rank between the two coalition partners. Higher-ranking female-female dyads formed coalitions more often than did lower-ranking dyads. Those female-female dyads that groomed more frequently also formed coalitions more frequently. The patterning of social interactions indicates that Cebus capucinus at Lomas Barbudal are female bonded. © 1996 Wiley-Liss, Inc.     

Infant Development and Parental Care in Free-Ranging <Emphasis Type="Italic">Aotus azarai azarai</Emphasis> in Argentina

Studies of infant development and parental behavior in free-ranging owl monkeys have been constrained by their nocturnal habits. Taking advantage of the cathemeral activity pattern of Aotus azarai azarai in the Argentinean Chaco, we describe the development of a cohort of free-ranging infants born in an owl monkey population in Formosa Province. We observed 7 infants, whose birth dates are known to the nearest week, to record details of their development and care between October 1999 and March 2000. We collected 92 h of behavioral data in 76 sessions. The infants were almost never off the parents during the first 4 wk of life, and we observed no infant being transported by a nonadult. The parent carrying the infant traveled most frequently in the middle of the group, sometimes first, but rarely last. The mean duration of 33 nursing episodes is 69 sec. After nursing, the infant was more likely to return to the nonnursing adult than to remain with the mother suggesting that in owl monkeys the infant may be primarily attached to the adult male in the group. Infants began to explore, to manipulate and to consume solid foods during the second month. Our observations are comparable to ones on captive breeding groups of Colombian owl monkeys (Aotus lemurinus) and Bolivian owl monkeys (A. azarai boliviensis) under controlled conditions of temperature, illumination and food availability.     

A test of the randomness of paternity of members of maternal sibships in six captive groups of rhesus monkeys (Macaca mulatta)

Results of previous studies have shown that in captive groups of rhesus monkeys (Macaca mulatto)fathers associate more frequently with their own offspring than with those of other males and that mothers are most permissive of physical contact between their own infant and a juvenile when that juvenile shares the same father with her infant. These two observations suggest that the identity of offspring born in captive groups of rhesus monkeys is recognized by at least some adult members of the group. Consistent patterns of mating among mating seasons might explain this apparent recognition of offsprings’ paternity. Fathers, for example, might regularly associate with young who maintain a close relationship with females with whom they have previously mated, and mothers might selectively permit juveniles who maintain a close relationship with males with whom they have previously mated to associate with their infants. This hypothesis is tested in this paper by comparing the observed distribution of 70 maternal sibships, members of which were fathered by the same or by different adult males over a 4-year period in six captive groups of rhesus monkeys, with that distribution expected based on random mating from season to season. Seasonal mating patterns were found to be random. Preparations are now underway to test this hypothesis in several free-ranging groups.     

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.     

The Influence of Age,Sex, and Rank on Yawning Behavior in Two Species of Macaques (Macaca fascicularis and M. fuscata)

Yawning behavior was studied in two species of macaques: the long-tailed macaque (Macaca fascicularis) and the Japanese macaque (M. fuscata). Japanese macaques yawned much more than long-tailed macaques. Age, sex, and dominance rank exerted different effects on yawning in the two species. In the long-tailed macaques, sex differences in frequency of yawning emerged only after sexual maturity; yawning rates increased significantly in both males and females as they reached sexual maturity; and, among males, dominance rank was positively correlated with frequency of yawning. Differently, in the Japanese macaques, males, both mature and immature, yawned more than same-aged females; sexual maturity was associated with an increase in yawning in males only; and male rank did not correlate with the frequency of yawning. Regardless of interspecific differences, the overall results supported only in part the finding that, in Old World monkeys, yawning is largely influenced by plasma concentrations of androgens. There was evidence that social factors were also important in influencing the age-sex class distribution of yawning.     

Changes in dominance rank and division of a wild Japanese monkey troop in Arashiyama

This article forms the second report on the Arashiyama troop of Japanese monkeys and concerns a troop division which took place in June, 1966, and various problems of rank and consanguinity which accelerated the division. (1) The hypothesis advanced in the first report has been verified; (2) at the time of troop division, several consanguineal groups formed one unit; (3) among 16 consanguineal groups, those from 1st to 7th in rank joined the A troop, while those from 8th to 16th joined the B troop; (4) dominance relation between the two division troops was B troop>A troop, reflecting the former ranking between the leader males of the two troops; (5) shifting of monkeys from one troop to the other after division occurred frequently, but males began to make their own movements when they attained 4 or 5 years of age and rarely moved together with their mothers or other consanguineous-relatives; (6) monkeys which were continuously in the same troop after division almost always obtained higher ranks than did monkeys who frequently shifted from one troop to the other; (7) after division, some males joined neither of the two division troops but formed a group, a so-called all-male group or male party, and moved about independently.