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.     

Food competition in captive female sooty mangabeys (Cercocebus torquatus atys)

We studied the social and foraging behavior of two captive groups of sooty mangabeys under two different spatial food situations. These food conditions were clumped (food was placed in a box) and dispersed (food was dispersed over the entire enclosure). In each group five adult females and two adult males were observed. As a criterion for food competition, individual differences in the relative food intake were used. Adult female mangabeys had a linear, stable, and unidirectional dominance hierarchy. Access to food was rank dependent among females only under clumped food distribution, as current models of the evolution of primate social systems predict. However, feeding success appeared to be mediated not by female but by male agonistic behavior toward females. High-ranking females received relatively less aggression from males and could, therefore, stay and feed longer in the feeding area. Male tolerance of higher-ranking females seems to mediate female feeding success under restricted food resources. The establishment of a special relationship with a high-ranking male might, therefore, be a strategy to get better access to food. This study demonstrates that female competition for access to food should not be analyzed separately from male influences on females and suggests that a more integral role of males in socioecological models of the evolution of primate social systems should be considered.     

Spontaneous gastric carcinomas in sooty mangabeys (Cercocebus atys)

Sooty mangabeys (Cercocebus atys) are native to West Africa and are a natural host of SIV, which is implicated in the origin of HIV2. They have been used in studies of AIDS pathogenesis, leprosy, immune responses, reproductive biology, and behavior. Spontaneous tumors have rarely been reported in this species. However, we noted spontaneous gastric carcinomas in 8 sooty mangabeys. Four male and 4 female mangabeys had mild to severe chronic weight loss, with abdominal distention in 5 of 8 animals. At necropsy, 7 of the 8 mangabeys had prominent large ulcerated masses with severe, diffuse thickening of the pyloric wall at or near the gastric-duodenal junction, which often partially occluded the gastric lumen. Early carcinoma was an incidental finding in one mangabey. Histologically, all of the tumors were classified as adenocarcinomas. Adenocarcinomas were noncircumscribed with infiltrates of neoplastic epithelial cells, often arranged in acini. In 3 mangabeys, these infiltrates were transmural and invaded surrounding tissue locally. The adenocarcinomas were locally invasive, with metastasis to regional lymph nodes in 2 animals, but widespread metastasis was not seen. Anisocytosis, anisokaryosis, and high mitotic rates were seen in all 8 tumors. In the samples available, serology and Steiner stain did not detect Helicobacter, and immunohistochemistry failed to reveal Helicobacter or Epstein-Barr virus, 2 potential causes for human gastric carcinomas.     

Infant carrying by adult male mangabeys (Cercocebus atys)

Sixty-five interactions where an adult male carried an infant in the proximity of a second male were observed during a 19-mo period in a captive sooty mangabey (Cercocebus atys) social group. The behavior was distributed nonrandomly in both the adult male and infant classes. In all but three of the interactions, the recently deposed alpha male carried an infant in the presence of the newly ascendant dominant male. In the first phase of the study, infants that were carried included the entire unweaned infant cohort (n = 5) born before the rank reversal. The rate of carrying in this class declined as a function of increasing infant age and time since the rank reversal. Infant carrying was not observed in the context of fighting, which was rare, and intermale aggression never preceded the behavior. However, in 40% of the cases, carrying occurred after an infant had been threatened by the dominant male. These results suggest that infant carrying served to protect the infant from aggression rather than to exploit the infant as an agonistic buffer. The data did not unequivocally support the postulate that carrying may be a form of paternal care since paternity could not be assessed. The similar structural and contextual patterns of infant carrying in this species suggest a common origin for triadic male-infant interactions in mangabeys and baboons.     

Female rank instability in newly formed groups of familiar sooty mangabeys (Cercocebus torquatus atys)

The formation of two new groups of sooty mangabeys (N=6; N=11) comprised of individuals removed from their natal group of 98 animals led to dominance rank challenges with aggression and wounding, though this occurred after an interval of months. Dominance rank challenges were not expected because, unlike rhesus macaques, adult female sooty mangabeys do not affiliate with adult kin significantly more than nonkin and show minimal agonistic aiding even with adult kin, thus rank would seem to be independent of aiding. Moreover, during the last nine years, severe wounding of adults in a large stable group of sooty mangabeys has been virtually absent and agonistic behavior in a stable group of sooty mangabeys is exhibited at a low rate compared to some macaque species. New members in the group of six maintained their relative ranks for 12 weeks after which the beta supplanted the alpha female with no serious wounding. This ranking remained stable for 29 weeks after which the alpha and beta females were supplanted with fatal wounds inflicted to the alpha and less severe wounds to the beta female. The second subgroup also kept their relative ranks initially. However, after 27 weeks the lowest ranking female severely wounded the next to last ranking female and 1 week later attacked and displaced the alpha female with minimal wounding. Fourteen weeks later the beta female (formerly the alpha) attacked and severely wounded the new alpha female and regained the top dominance position. These events suggest that although sooty mangabeys do not exhibit strong kin preferential behavior among adults, they do have defined relationships within the long term, stable group. Removal from those defined relationships allows the possibility of social reorganization that may be mediated by serious aggression.     

Hard-object feeding in sooty mangabeys (Cercocebus atys) and interpretation of early hominin feeding ecology

Morphology of the dentofacial complex of early hominins has figured prominently in the inference of their dietary adaptations. Recent theoretical analysis of craniofacial morphology of Australopithecus africanus proposes that skull form in this taxon represents adaptation to feeding on large, hard objects. A modern analog for this specific dietary specialization is provided by the West African sooty mangabey, Cercocebus atys. This species habitually feeds on the large, exceptionally hard nuts of Sacoglottis gabonensis, stereotypically crushing the seed casings using their premolars and molars. This type of behavior has been inferred for A. africanus based on mathematical stress analysis and aspects of dental wear and morphology. While postcanine megadontia, premolar enlargement and thick molar enamel characterize both A. africanus and C. atys, these features are not universally associated with durophagy among living anthropoids. Occlusal microwear analysis reveals complex microwear textures in C. atys unlike those observed in A. africanus, but more closely resembling textures observed in Paranthropus robustus. Since sooty mangabeys process hard objects in a manner similar to that proposed for A. africanus, yet do so without the craniofacial buttressing characteristic of this hominin, it follows that derived features of the australopith skull are sufficient but not necessary for the consumption of large, hard objects. The adaptive significance of australopith craniofacial morphology may instead be related to the toughness, rather than the hardness, of ingested foods.     

Sex differences in behavior of endangered mangabeys (Cercocebus galeritus chrysogaster)

Six adult golden-bellied mangabeys (Cercocebus galeritus chrysogaster) displayed sex differences in aggression, grooming, and vocalization. These sex differences persisted across different current living conditions, time in captivity, rearing conditions, presence of offspring, and active mating conditions. The sex differences are evidently quite robust.     

Hormones and sexual behavior associated with postconception perineal swelling in the sooty mangabey (Cercocebus torquatus atys)

Three studies were conducted with female sooty mangabeys to describe the occurrence of perineal swelling during pregnancy and to document the associated patterns of ovarian hormone secretion and sexual behavior. Menstrual cycles and pregnancies were charted in 29 female subjects by recording daily vaginal bleeding and perineal swelling. As in other swelling species, maximum perineal tumescence corresponded with the periovulatory phase of the cycle; however, a second tumescence was recorded during pregnancy, with a peak at 49 days postconception. The swelling patterns were similar with the exception that deturgescence was slower during pregnancy. In a second study, blood samples were obtained weekly from nine females to document the estradiol (E₂) and progesterone (P₄) profiles during pregnancy. Analyses revealed increased E₂ concentrations and low P₄ levels in association with the postconception swelling. A third study compared sexual behavior during ovulatory and post-conception tumescent peaks. Behavioral data revealed that, although there was no overall difference in male mount rate to females during the ovulatory and postconception maximum swelling period, when only the alpha male was considered, significantly fewer mounts were directed to females exhibiting a post-conception versus an ovulatory maximum tumescence.     

Developmental patterns of serum luteinizing hormone, gonadal and adrenal steroids in the sooty mangabey (Cercocebus atys)

Serum levels of luteinizing hormone (LH), testosterone, dehydroepiandrosterone sulfate (DHAS), androstenedione and cortisol were determined in multiple samples from 86 sooty mangabeys of varying ages (0-17 years). Testosterone, androstenedione, DHAS and cortisol were measured by radioimmunoassay; LH was determined by in vitro bioassay. Serum LH concentrations were elevated in neonates (less than 6 months) and in animals older than 72 months of age. The higher LH levels were associated with increased circulating concentrations of testosterone in males but not females. The pubertal rise in serum testosterone at approximately 55-60 months of age in males was coincident with rapid body growth. No pubertal growth spurt was observed in females. Serum levels of androstenedione and DHAS were highest during early postnatal life (less than 6 months) with androstenedione exceeding 600 ng/dl in males and 250 micrograms/dl in females, but declined rapidly in both sexes to a baseline of 150 ng/dl by 19 months of age. Serum androstenedione did not fluctuate significantly in adult animals. The pattern of age-related changes in serum DHAS paralleled those of serum androstenedione, whereas serum cortisol values did not change significantly with age. Developmental changes in serum LH, testosterone and body weight suggest that the sooty mangabey matures substantially later than the rhesus monkey. The pattern of serum gonadal and adrenal steroids during sexual maturation is similar to that seen in the baboon with no evidence of an adrenarche.     

Isolation and characterization of the first simian immunodeficiency virus from a feral sooty mangabey (Cercocebus atys) in West Africa

Abstract: The lineage of HIV-2-like viruses was studied in feral sooty mangabeys (SMs) by serological and genetic methods. Four feral sooty mangabeys were positive for simian immunodeficiency virus (SIV) antibodies and a new isolate, SIV_smSL92a, was obtained. Genetic analysis of gag genes showed that SIV_smSL92a was highly diverse and a distinct sequence subtype within the SIV_sm/HIV-2 family. The results showed that SIV_sm is the most diverse group of SIVs found thus far in a single monkey species.     

A brief report on the social behavior of the crested mangabey (Cercocebus galeritus galeritus) with a comparison to the sooty mangabey (C. torquatus atys)

A group of 38 free ranging crested mangabeys in the Tana River Primate Reserve was studied over a 6-week period for a total of 209.5 hr and behavioral comparisons made to a captive group of sooty mangabeys. Although quantitative comparisons between these two mangabey species are not possible, the present data suggest that these geographically separated mangabeys share several behavioral similarities. Copulatory behavior in both species involved a pattern of female darting and female vocalizing following the mount by the male. Several similarities in agonistic behavior also existed: 1) The victim often returned or stayed within 1 m of the aggressor following an agonistic episode; 2) retaliation in which the victim first fled or avoided the aggressor, then subsequently, chased or lunged at the aggressor, typically while screaming; and 3) frequent redirection of aggression by the victim following an agonistic episode. A dominance rank reversal occurred between the two adult male crested mangabeys with no severe wounding. The rank reversal seemed to be related to two subsequent behaviors which included infant carriage by the deposed alpha in the presence of the new alpha male and female demonstrations of extreme protectiveness of their infants in the presence of the new alpha male. Both of these behaviors have been reported in the sooty mangabey group.     

Peaceful primates: affiliation, aggression, and the question of female dominance in a nocturnal pair-living lemur (Avahi occidentalis)

Affiliation/agonism and social dominance are central factors determining social organization in primates. The aim of our study is to investigate and describe, for the first time, the intersexual relations in a nocturnal and cohesive pair‐living prosimian primate, the western woolly lemur (Avahi occidentalis), and to determine to what extent phylogeny, activity mode, or the cohesiveness of pair partners shape the quality of social interactions. Six pairs of western woolly lemurs were radio‐collared in the dry deciduous forest of northwestern Madagascar. More than 874 hr of focal animal sampling were conducted. All occurrences of social interactions involving a focal animal were recorded. The rate of affiliation between pair partners was significantly higher than the rate of agonism. Western woolly lemur pairs' interactions were extremely peaceful. All decided agonistic conflicts (N = 15) were exclusively initiated and won by the female. No female showed spontaneous submission toward her male partner. These results are in line with those of diurnal cohesive pair‐living anthropoid primates. Findings support the hypothesis that social relations in pair‐living primates are linked to the cohesiveness of pair partners in time and space irrespective of phylogeny and activity mode. Am. J. Primatol. 73:1261–1268, 2011. © 2011 Wiley Periodicals, Inc.     

Female grooming markets in a population of gray-cheeked mangabeys (Lophocebus albigena)

Primate female allogrooming models based on biological marketstheory predict that grooming is "time matched" within bouts,that is, the amount of time the first female grooms predictsthe amount of time the second one grooms. The models also predictthat when female–female contest competition is weak, groomingis traded for grooming, but when female–female contestcompetition is strong, grooming may be traded for other commoditiessuch as feeding tolerance, and grooming discrepancy betweenmembers of dyads is rank related. We tested these predictionsusing data collected from adult and subadult female gray-cheekedmangabeys (Lophocebus albigena) (N = 26) in 5 groups in KibaleNational Park, Uganda. We found that, overall, females reciprocatedin 33% of grooming bouts. Among reciprocated bouts, femalesin all 5 groups showed time matching. In 2 groups, we also foundrank-related grooming discrepancies but showing opposite patternsto each other. Consistent with predictions based on biologicalmarkets theory, these groups may have been under greater feedingcompetition, revealed more by adjustments in ranging behaviorthan increased agonistic rates. Although these results supportcurrent allogrooming models, they also suggest that the modelsmay become more robust if the influence of scramble competitionis incorporated. In addition, they emphasize the flexibilityand dynamic nature of female competitive relationships withinthe same population of primates.     

Agonistic and Affiliative Relationships of Adult Female Howlers (Alouatta palliata) in Costa Rica Over a 4-Year Period

We observed 12 adult female mantled howlers (Alouatta palliata), which have been part of Group 2 at Hacienda La Pacifica, Guanacaste Province, Costa Rica, via focal animal sampling during portions of July and August of 1988 and 1990–1992 (7–9 females/year, 955.3 hr of observation). We used agonistic interactions and time in proximity (<1 m) as indices of social relationships. The rate of female–female agonistic interactions was 0.38/hr (yearly range: 0.24 to 0.51/hr). Yearly dominance hierarchies, based on outcomes of dyadic agonistic interactions, varied in linearity between 60.7 and 94.6%. Adult females spent 7.10% of their time in proximity to another adult female (yearly range: 1.04–15.64%) and 4.95% of their time in proximity to an adult male (yearly range: 2.27–7.51%). Using yearly dominance ranks, we tested proximity patterns for differences based on rank and presence of dependent offspring. In 3 of the 4 years, high-ranking females spent significantly greater proportions of their time in proximity with other females than did low-ranking females. Time in proximity with the 3 or 4 adult males was not associated with rank. Having a dependent infant was not related to the proportion of time in proximity to females or males, and females, especially top-ranking ones, spent more time in proximity to females with dependent infants than to females without infants. These results show that social relationships in mantled howler groups are dynamic and generally support predictions made by von Schaik (1989) regarding scramble-type, female competitors. We also discuss the roles of immigrations, infants, and male relationships in the patterning of social relationships.     

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.     

Validation of radioimmunoassays for LH and FSH in the sooty mangabey (Cercocebus atys): Characterization of LH and the response to GnRH

Heterologous radioimmunoassays (RIA) for macaque LH and FSH were validated for the measurement of these hormones in the sooty mangabey and mangabey pituitary LH was characterized relative to rhesus monkey LH. Dilutions of a pituitary mangabey extract and a partially purified preparation of mangabey LH ran parallel to a rhesus monkey standard (LER 1909-2) in the ovine-ovine (o-o) LH assay but showed some deviation from parallelism in the rhesus monkey FSH assay. The LH potency of the mangabey extract and standard were six and 190 times more potent, respectively, than LER 1909-2 in the LH RIA. Mangabey LH was estimated to have a molecular weight of 40,000–42,000 daltons vs 35,000–38,000 daltons for rhesus LH on Sephadex G-100 chromatography. Plasma levels of radioimmunoreactive LH, FSH, and testosterone were assayed before and after a bolus administration of 25, 50, or 100 μg synthetic go-nadotropin releasing hormone (GnRH) to adult male mangabeys. A significant increase in serum levels of LH was seen within 30 min with levels more than fourfold higher than the basal level of LH after administration of 100 μg GnRH. However, no consistent increases in plasma FSH values were detected. The integrated mean LH response above preinjection levels following 25, 50, or 100 μg GnRH was dose related. Serum levels of testosterone were also elevated after administration of GnRH, but peak concentrations of testosterone lagged behind peak levels of LH by approximately 30 min. These studies indicate that the heterologous RIAs may be used for measuring gonadotropins in the mangabey and that the male mangabey is apparently more sensitive to GnRH than the rhesus monkey.     

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.     

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.     

Sexual selection in gallus: Effects of morphology and dominance on female spatial behavior

Sexual selection has received a great deal of attention from field and laboratory researchers for over a century, but hard evidence of female choice of mates in mixed-sex groups remains scarce. Dominant males typically mate much more often than subordinants but evidence that females “choose” such males is elusive. In $\text{Gallus}$, which includes junglefowl and their domestic fowl descendants, females stay near and mate with dominant, territorial males. We demonstrate here that $\text{Gallus}$ females in mixed-sex flocks who have no information about the social dominance status of males orient to, approach and stay near males with larger than average combs whereas females which $\text{do}$ not have information about male dominance orient toward and stay near high ranking males. We verify that comb size correlates with male social rank. Hence, $\text{Gallus}$ females do actively respond to “high quality” males; they apparently identify such males by male physical characteristics and, if available, information concerning male-male interactions.     

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.