Within-group social bonds in white-faced saki monkeys (Pithecia pithecia) display male-female pair preference

White‐faced saki monkeys (Pithecia pithecia) lack most of the behavioral and physical traits typical of primate monogamy [Fuentes, 1999 ]. In order to determine if social bonds in this species reflect patterns displayed by pair‐bonded groups or larger multimale–multifemale groups, we draw on 17 months of data collected on wild white‐faced sakis at Brownsberg Nature Park, Suriname. We analyzed within‐group social bonds for three habituated groups (one two‐adult and two multiadult groups) by measuring grooming, proximity, and approach/leave patterns between adult and subadult group members. We found that both two‐adult and multiadult groups showed significantly stronger social bonds between a single male–female dyad within each group (deemed “primary dyads”). In all three groups, primary dyads were composed of the oldest adult male and a breeding female. These pairs had significantly higher levels of grooming than other within‐group dyads and were also in close proximity (<1 m) more often than nonprimary dyads. Grooming in primary dyads was nonreciprocal, and consistently biased toward female investment. Grooming patterns in nonprimary dyads varied, but were often more reciprocal. Grooming and proximity of the primary dyad also changed in relation to infant development. Our results suggest that while white‐faced sakis do not show behavioral and physical traits typical of monogamy or pair‐bonding, social bonds are strongest between a single male–female pair. Pitheciine social systems range from small group monogamy in Callicebus to large multimale–multifemale groups in Chiropotes and Cacajao. As the middle taxon in this platyrrhine radiation, behavioral strategies of white‐faced sakis provide a model for how social bonds and affiliation could be influenced by and affect the evolution of larger group size in primates. Am. J. Primatol. 73:1051–1061, 2011. © 2011 Wiley‐Liss, Inc.     

Social behavior of captive,group-living Orangutans

The behavior of orang-utans (Pongo pygmaeus)was observed in two captive groups (one adult group, one juvenile group). Activity profiles,animal interactions, and compartmental spatial use for both adult-group and juvenile-group individuals were recorded over a 9-month period. Behavioral repertoires for both groups included large amounts of social activity. Equivalent amounts of social activity were found for each group. The social behavior of juvenile animals involved more active behavior such as play. The social behavior of the adult animals was more subtle, involving social monitoring and allogrooming. These results indicate that orangutans, at least when group-living in captivity, exhibit the potential to display social behavior which is apparently of greater frequency and complexity than that which has been observed in the wild. These findings suggest that the solitary behavior of wild orangutans is not a necessary characteristic of orangutan behavior. Under different environmental conditions orangutans appear to readily adapt socially, and, like other nonhuman primates,they have the capacity to exhibit complex and subtle social behavior. This report is based on part of a senior thesis submitted by Sara D. Edwards     

Social behaviour and infant carrying in a group of moustached tamarins,Saguinus mystax (primates: Platyrrhini: Callitrichidae), on Padre Isla,Peruvian Amazonia

The social behaviour of a group of eight moustached tamarins,Saguinus mystax, (five males, three females) was studied on Padre Isla in northeastern Peru. About 60% of all allogrooming was done by the two adult males in the group, and about 11% by a young adult female. All other group members groomed very little. The adult breeding female received more grooming than any other group member. After the death of the adult female (preyed upon by an anaconda) the amount of active allogrooming remained constant for all group members except for the young adult female, who increased her contribution to about 30%. Her preferred grooming partner was the subadult female, which generally screamed when being groomed by the young adult female and terminated grooming by going away. This kind of grooming relation is termed “forced grooming” and is interpreted as a possible social control mechanism. The young adult female groomed the adult males more often after the death of the adult female than before. This might have had the function of strengthening the social bond with the adult males and in obtaining the breeding position in the group. After the death of the adult female, the vulva of the young adult female grew to full adult size. Agonistic behaviour was less frequent than allogrooming. Most aggressive interactions (50%) originated from the subadult male of the group. The young adult female was the target of most of these aggressions. Extremely little aggression occurred between the three females. The young adult female was the only individual who tried to emigrate from the group during the study period. Her attempt to join a neighbour group failed due to rejection by all four members of this group. All group members participated in carrying an infant, but the adult males and the young adult female carried most frequently. Contribution to infant carrying varied with the infant's age.     

Social influences on first reproductive success and related behaviors in the saddle-back tamarin (Saguinus fuscicollis,callitrichidae)

Some aspects of sociosexual behavior and the age at which maturing females experienced their first evident pregnancy and at which maturing males caused their first evident pregnancy were recorded in Saguinus fuscicolliscohabiting from 6 months of age with either an adult or a maturing sex partner. The following pair combinations and trios were studied: young male -young female, young male-adult female, adult male-young female, and adult male-young male-young female. The most frequent type of social interaction between young animals was rough and tumble play, while huddling was the most frequent interaction between young animals and their adult partners. Grooming and sexual interactions were very infrequent and there were no differences in the frequencies of these interactions among subject groups. Maturing females cohabiting with an adult male conceived significantly earlier than maturing females cohabiting with a male of their own age. Maturing males cohabiting with adult females sired offspring at a significantly earlier age than males cohabiting with a female of their own age. Some possible behavioral and physiological processes involved in the causation of early reproductive success in young tamarins cohabiting with adults are discussed. Saguinus fuscicollis fuscicollis andSaguinus fuscicollis illigeri.     

Allogrooming behavior inCercocebus torquatus: The case for the hygienic functional hypothesis

The hygienic functional hypothesis of allogrooming behavior was examined in two captive groups (N=9 andN=8) of white-crowned mangabeys (Cercocebus torquatus lunulatus) by analyzing: (1) the corporal distribution of manipulation type according to hair density, and (2) the corporal distribution of allogrooming according to presence of wounds. In both groups the sites with higher hair density received more bouts of Superficial Grooming, which implies a tactile screening of a fragment of the body surface. Only one group tended to emit more allogrooming on the body sites when they were wounded. In the other group, however, the number of wounds was very small and the wounds concentrated predominantly on those sites which were accessible to the subject itself. Thus, our results may be consistent with the hygienic functional hypothesis of allogrooming behavior in general and with the sanitary one in particular.     

A field study of the ecology and behavior of the black-mantle tamarin (Saguinus nigricollis)

The author made an ecological study of the black-mantle tamarin (Saguinus nigricollis) in the primary forest in the basin of the River Caquetá in the upper Amazon in Colombia for 88 days during a study period from August 1975 to February 1976. The tamarin group repeats three activity patterns — feeding, resting, and moving — regularly in a day. In their feeding activity, the tamarins preferred to eat small insect and resin. They showed a special liking for large grasshoppers, 6–8 cm long, and spent much of the day to capture them. Moving in search of the grasshoppers, which are hard to capture in the forest, is closely related to the tamarin group's daily nomadism. From this evidence it can be concluded that the behavior which forms the basis of the tamarins' daily activity is the hunting of grasshoppers. In the transition time from the feeding activity, principally the hunting of grasshoppers, to the resting activity, a fruit eating behavior was always observed. At this time the tamarins ate well-ripened sweet fruit intensively for a short time. This behavior is thought to have the effect, in one respect, of easing strained relations arising among group members during the grasshopper hunting activity. It was also observed that mother tamarins shared their hard-to-capture grasshoppers with their offspring although the latter had already become independent of their mothers. In general, the tamarins lived in a small and compact group consisting of an adult male, an adult female, and their offspring. Some of these small groups had amicable interrelationships and often moved together, whereas other groups kept aloof from each other. These facts indicate that, besides the groups as the social units, large-groups comprising some of these unit groups moving together, exist in the social structure of the tamarins, and form the upper structure of the social unit. See the note added to the end of this article.     

The effect of social environment on estrogen excretion,scent marking,and sociosexual behavior in tamarins (Saguinus oedipus)

The influence of various social environments on estrogen excretion, scent marking, and the expression of sociosexual behavior was examined in cotton-top tamarins (Sanguinus o. oedipus). Behavioral observations and urine collections were conducted on five females while first housed in their natal family group or in the presence of another cycling adult female and then while housed with an unrelated adult male in a separate cage. Behavioral observations only were conducted on males in natal family groups and while housed with an unrelated adult female. Levels of urinary estrone and estradiol for females were measured by specific radioimmunoassays. Females housed in family groups or in the presence of an adult cycling female showed low and noncyclic patterns of estrogen excretion. Removal from these environments resulted in a rapid increase in urinary estrone and estradiol and three of five females demonstrated cyclic patterns of estrone excretion. Rates of anogenital marking in females were elevated after the social change, and sexual interactions, virtually absent in the original environments, were observed in all five females. In males, similar manipulations of the social environment affected the expression of sexual behavior, but not scent marking. The social environment, therefore has a profound impact on fertility and sociosexual behavior in cotton-top tamarin groups, with implications for callitrichid social structure and behavior.     

Social and seasonal influences on reproductive biology in male moustached tamarins (Saguinus mystax)

In several primate taxa there is evidence that the social and physical environment can exert a significant effect on reproductive behavior and biology. In this paper we examine social and physiological factors influencing group composition and reproduction in free-ranging moustached tamarin monkeys (Saguinus mystax mystax). This species is characterized by cooperative care of the young and a breeding system that includes both polyandrous and polygyandrous matings. Body measurements collected on adult males residing in multimale groups indicate marked within-group differences in testes volume. In 12 of 17 groups examined, testes volume of at least two resident adult males differed by 21–174%. Among these males, testes volume was not correlated with either body weight or adult age class. We also examine whether factors such as time of year had an effect on reproductive condition. An analysis of body measurements of 128 adult male and 127 adult female moustached tamarins, wild-trapped and released in northeastern Peru, indicates cyclic changes in genital size. For males, mean monthly testes volume in July (712 mm³) was twice that recorded in June (351 mm³). Females exhibited a similar pattern. Although endocrine information on intra- and intersexual social effects on fertility are unavailable for S. mystax, given the high degree of social cooperation and lack of overt aggression among adult male group members, we offer the possibility that resident male moustached tamarins compete for access to the groups' lone breeding female through socially induced reproductive suppression and sperm competition. © 1996 Wiley-Liss, Inc.     

Acute changes in social composition and agonistic behavior in male vervet monkeys (Cercopithecus aethiops sabaeus)

Among nonhuman primates the composition of social groups influences the interactions of group members. We assessed the effects of acute changes in social composition on behavior among 15 adult male vervet monkeys (Cercopithecus aethiops sabaeus). Subjects were observed in their basal social groups which comprised 3 adult males, 2–4 adult females, and offspring; and in two subgroups consisting of either two or three adult males. Agonism and vigilance increased in smaller groups relative to basal conditions, while subjects in two-male groups displayed more aggression than those in three-male groups. These findings suggest that, among male vervet monkeys, acute disruption of stable social groups increases aggressive behavior, and that the amount of agonism is influenced by the composition of the consequent subgroups. © 1992 Wiley-Liss, Inc.     

Allogrooming Behavior and Grooming Site Preferences in Captive Bonobos (Pan paniscus): Association with Female Dominance

I tested the utility of Seyfarth's (1977) model of rank-related attractiveness to explain the distribution of allogrooming behavior among captive bonobos (Pan paniscus). Adult female bonobos generally have high social status and may be dominant over males. As predicted by the model, I found that high-ranking adult females received most allogrooming within each of the four investigated groups. Among adult female-adult female dyads, however, allogrooming was not clearly associated with dominance rank. Contradictory to predictions of the model, the highest-ranking females were responsible for most displacements over allogrooming, and grooming competition is positively correlated with dominance rank. In the second part of this study, I investigated the social significance of allogrooming body site preferences. Bonobos direct significantly most allogrooming to the face of conspecifics, and high- and low-ranking individuals, as well as males and females, differ significantly in their preferences for certain allogrooming sites. Subordinates and males tended to avoid facial grooming and preferred the back and anogenital region, while high-ranking individuals and females directed most allogrooming to the face and head of grooming partners. Data from this study support the hypothesis that high-ranking females are the most attractive grooming partners within a female-centered bonobo society. Many other aspects of allogrooming behavior, however, are not consistent with the model of rank-related attractiveness.     

Grooming in brown howler monkeys,Alouatta fusca

The grooming behavior of a group of brown howler monkeys was studied for one year in an Atlantic forest reserve of southeastern Brazil. A total of 290 grooming bouts were recorded and analyzed. The two adult females directed most of the grooming (91%), while the adult male was the major recipient (37%). Grooming between females, and between them and their siblings, also occurred quite often. On average, the group spent 2% of its daily time grooming, with a higher frequency around noon. There were significant differences, however, in time spent grooming between seasons; grooming was more abundant during the coldest seasons (autumn–winter) and rarer in hotter ones (spring–summer). A significant negative correlation was found between grooming time and temperature, but contrary to expectations, grooming time failed to correlate with both the group' diet and the demands of food-gathering, as measured by travelling time and day range length. A comparison of grooming behavior with other species of the genus suggests that brown, red (A. seniculus), and black howler monkeys (A. caraya) are more similar to each other than to mantled howlers (A. palliata), a result that probably is linked with the differing social structure and group size of the latter species. © 1995 Wiley-Liss, Inc.     

Social grooming in Tonkean macaques (Macaca tonkeana)

The distribution, form, and contexts of occurrence of social grooming were studied in two captive groups of Tonkean macaques (Macaca tonkeana), using interaction-dependent sampling. The social events surrounding grooming had little influence on its form, the participants' behavior being shaped mainly by physical constraints. Adult females were most often involved in grooming interactions. Grooming between adult females appeared more intimate than that between adult males and females. Kinship and dominance had no effect on the form or distribution of social grooming among adult females. It is concluded that social systems that are characterized by mild dominance relations allow individuals the freedom to interact in the way and with whom they wish.     

Relation of Intergroup Variation in Allogrooming to Group Social Structure and Ectoparasite Loads in Red Howlers (Alouatta seniculus)

We compare the allogrooming behavior of 5 troops (average size = 8.2) of red howlers (Alouatta seniculus) from the Venezuelan Llanos with that of other A. seniculus and Alouatta spp. of the genus. In 126.9 observation hr, we recorded 118 allogrooming events, with an average bout length of 109 sec. Females groomed more frequently than males did, but as groomees there is no significant differences between sexes. Adult males groomed adult females mostly in a sexual context (before copulation). Allogrooming rates differ significantly among groups. There are also significant differences among members of the same troop both as groomers and groomees, which we explain in the context of the social behavior and history of each troop. There is no significant correlation between weight of the groomee and duration of the grooming bout. However, the examination of grooming rates and ectoparasite load suggests that allogrooming may have hygienic consequences. Differences in allogrooming rates among species of Alouatta are related to differences in group kin structure and patterns of female competition, in particular, coalition formation. We conclude that the social structure and the degree of relatedness among individuals within a group (or among individuals in a population in interpopulation comparisons) is a more important determinant of allogrooming rate than body size or group size. Our results emphasize the importance of considering intergroup and interpopulational variation in behavior.     

Intragroup Social Relationships of Male Alouatta palliata on Barro Colorado Island,Republic of Panama

We examined social and spatial relations of adult males in one group of mantled howling monkeys (Alouatta palliata) on Barro Colorado Island (BCI) in central Panama to document patterns of association. Beyond the existence of an alpha male, we could not distinguish any linear dominance hierarchy among the 6 study males. All males copulated with estrous females. Our findings contrast with reports of intragroup male behavior in Costa Rican howlers. Study males engaged in little or no affiliative or agonistic behavior with one another, but engaged in significantly more such interactions with females. The alpha male, the oldest male and a younger male were most frequently in association with females. Of group males, the oldest male associated significantly more with other males. Overall, male behavior in mantled howling monkeys on BCI generally followed the van Hooff and van Schaik (1994) model of male relationships. The low incidence of intragroup social interactions of any type in the focal males may reflect the energetic costs of social behavior. We suggest that intragroup social relationships among mantled howler males are structured by more subtle means than overt physical interactions, possibly including vocal communication, relationships with individual group females, and kinship.     

Demography,group composition,and dispersal in wild cotton-top tamarin (Saguinus oedipus) groups

Groups of individually marked cotton-top tamarins (Saguinus oedipus), located in La Reserva Forestal Protectora Serranía de Coraza-Montes de María in Colosó Colombia, were studied over a period of 5 years. Data on group composition, stability, birthing seasons, and dispersal patterns are used to examine the reproductive strategies and tactics used by males and females. Both monogamous groups and groups containing two pregnant females have been observed. All groups contained at least one adult female and male, with several groups containing several adult males and females. Both males and females dispersed to neighboring groups, and there were no sex differences in rates of emigration. Males were more likely to immigrate into a new group following the death/emigration of a resident male. Females appeared to tolerate immigrating females but would actively defend their breeding position during fertile periods. © 1996 Wiley-Liss, Inc.     

Pattern, Distribution, and Function of Greeting Behavior Among Black-and-White Colobus

Various species of primates engage in greeting, a ritualized pattern of nonaggressive behavior that usually occurs during a reunion. Black-and-white colobus (Colobus guereza) perform overhead mounting, mounting, and embracing behavior soon after an aggressive act and in nonagonistic situations. We studied the pattern, distribution, and function of the greeting behavior in 2 captive groups of black-and-white colobus. Overhead mounting was the most frequent pattern, accounting for >60% of all greetings (N=333). In nonagonistic situations, younger subordinate individuals greeted an older dominant individual more frequently than vice versa. A dominant male in a small multimale group frequently initiated contacts with adult females, though he was the oldest in the group. Conversely, the dominant male in a large 1-male group never greeted group members. Immediately after performing the greeting, the greeter groomed the recipient in more than half the cases. In the large group, greeting frequency correlates positively with the age difference between the pair; however, there is no correlation between the relatedness, affiliation frequency, or aggression frequency of a pair in either the small or large group. The results are consistent with the hypothesis that greeting behavior functions as a tension-reducing mechanism in nonagonistic situations. There is no evidence, however, that greeting functions to express social status or to attract a mate. In addition, the frequent greeting by the adult male in the small multimale group may indicate that individuals affirm social bonds via greeting behavior.     

Grooming relationships between breeding females and adult group members in cooperatively breeding moustached tamarins (Saguinus mystax)

Grooming is the most common form of affiliative behavior in primates that apart from hygienic and hedonistic benefits offers important social benefits for the performing individuals. This study examined grooming behavior in a cooperatively breeding primate species, characterized by single female breeding per group, polyandrous matings, dizygotic twinning, delayed offspring dispersal, and intensive helping behavior. In this system, breeding females profit from the presence of helpers but also helpers profit from staying in a group and assisting in infant care due to the accumulation of direct and indirect fitness benefits. We examined grooming relationships of breeding females with three classes of partners (breeding males, potentially breeding males, (sub)adult non-breeding offspring) during three reproductive phases (post-partum ovarian inactivity, ovarian activity, pregnancy) in two groups of wild moustached tamarins (Saguinus mystax). We investigated whether grooming can be used to regulate group size by either "pay-for-help" or "pay-to-stay" mechanisms. Grooming of breeding females with breeding males and non-breeding offspring was more intense and more balanced than with potentially breeding males, and most grooming occurred during the breeding females' pregnancies. Grooming was skewed toward more investment by the breeding females with breeding males during the phases of ovarian activity, and with potentially breeding males during pregnancies. Our results suggest that grooming might be a mechanism used by female moustached tamarins to induce mate association with the breeding male, and to induce certain individuals to stay in the group and help with infant care.     

Influences of Relatedness,Food Deprivation,and Sex on Adult Behaviors in the Group‐living Insect Forficula auricularia

The evolution of group living is generally associated with the emergence of social behaviors that ensure fitness benefits to group members. However, the expression of these behaviors may depend on group composition, which can vary over time with respect to sex, starvation status, and relatedness. Here, we investigated (1) whether adults of the group‐living European earwig, Forficula auricularia, show cooperative behaviors toward conspecifics and (2) whether sex, food availability, and relatedness shape the nature and frequency of these behaviors. We conducted a full‐factorial experiment using 108 unisexual pairs of adults, in which we manipulated these three factors and video‐recorded the earwig behaviors for 45 min. Our results revealed that adults mostly expressed self‐directed and aggressive behaviors. Nevertheless, they also showed allogrooming, a social behavior that offers scope for cooperation. Pairs of males displayed longer bouts of aggression and allogrooming (when it occurred) than pairs of females. Food deprivation had no effect on male behaviors, but females spent less time self‐grooming and walking when they were food deprived. Finally, low relatedness between adults did not influence any of the measured behaviors, but exacerbated frass production, possibly due to social stress. Overall, these results indicate the limited role of cooperation among F. auricularia adults during their group‐living phase.     

Maintenance of Multifemale Social Organization in a Group of <Emphasis Type="Italic">Nomascus concolor</Emphasis> at Wuliang Mountain,Yunnan, China

Many short-term studies have reported groups of black crested gibbons containing ≥2 adult females (Nomascus concolor). We report the stability of multifemale groups in this species over a period of 6 yr. Our focal group and 2 neighboring groups included 2 breeding females between March 2003 and June 2009. We also habituated 1 multifemale group to observers and present detailed information concerning their social relationships over a 9-mo observation period. We investigated interindividual distances and agonistic behavior among the 5 group members. The spatial relationship between the 3 adult members (1 male, 2 females) formed an equilateral triangle. A subadult male was peripheral to the focal group, while a juvenile male maintained a closer spatial relationship with the adult members. We observed little agonistic behavior among the adult members. The close spatial relationship and lack of high rates of agonistic behavior among females suggest that the benefits of living in a multifemale group were equal to or greater than the costs for both females, given their ecological and social circumstances. The focal group occupied a large home range that was likely to provide sufficient food sources for the 2 females and their offspring. Between March 2003 and June 2009, 1 adult female gave 2 births and the other one gave 1 birth. All individuals in the focal group survived to June 2009. A long-term comparative study focused on females living in multifemale groups and females living in pair-living groups would provide insight into understanding the evolutionary mechanisms of the social system in gibbons.     

Demographic and reproductive patterns in moustached tamarin monkeys (Saguinus mystax): Implications for reconstructing platyrrhine mating systems

In this paper we address a series of questions concerning reproductive opportunities, kinship, dispersal, and mating patterns in free-ranging moustached tamarin monkeys (Saguinus mystax). Between 1980 and 1990 information on group size, composition, and migration patterns was collected on marked groups of moustached tamarins inhabiting Padre Isla, an island in the Amazon Basin of northeastern Peru. In 1990, 86% of 114 animals residing in 16 social groups were trapped, examined, and released. Mean group size was 7.0, including 2.2 adult males and 2.0 adult females. None of these groups was characterized by a single adult male-female pair. In groups with more than one adult female, only the oldest female produced offspring. An examination of dispersal patterns indicates that transfers between groups were common and fell into several categories, including immigration of individual males and females, simultaneous transfer of pairs of subadult and/or adult males (sometimes relatives) into the same social groups, and group fissioning in which males and females of the splinter group join another small social group. We have no unambiguous cases of 2 adult/subadult females migrating together into the same social group. All 6 groups for which reproductive data were available were characterized by either a polyandrous or polygynous (polygyandrous) mating pattern. The results of this study indicate that moustached tamarins reside in small multimale multifemale groups that are likely to contain both related and unrelated adult group members. Kinship and social ties among males appear to be stronger and more longlasting than kinship and social ties among females. We contend that the modal mating system of moustached and many other tamarins is not monogamous, and offer the possibility that cooperative infant care and mating system flexibility in callitrichines evolved from a polygynous mating pattern. © 1993 Wiley-Liss, Inc.