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.     

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.     

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.     

Attacks on neonates by a male mangabey (Cercocebus atys)

Aggressive behavior by an adult male toward selected infants and their mothers was observed during a long-term study of reproduction in a captive social group of sooty mangabeys (Cercocebus atys). The highest-ranking adult male in this group was observed to attack and bite three neonates out of a total of 13 infants born in 1982. All three attacks were directed attacks in which infants were grabbed from their mothers and bitten in the head. The first infant was fatally injured; the other two probably would have sustained fatal wounds had the male's canines not been blunted beforehand and had observers not intervened. The attacks were preceded by a pattern in which the male persistently stalked or chased the mother-infant pairs, a behavior first observed in the hours immediately following parturition. Unlike attacks in wild baboon groups following male immigration, these attacks on infants occurred in a stable social group in which the male attacker had been a lifelong resident. This male, however, had gained alpha rank only 3 months before attacking the first infant. These attacks, in the context of other evidence of aggression and wounding, are discussed relative to current models of infanticide in primates.     

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.     

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.     

Hormonal correlates of ontogeny in baboons (Papio hamadryas anubis) and mangabeys (Cercocebus atys)

This study investigates the relationship between serum hormone levels and morphometrics during ontogeny in olive baboons (Papio hamadryas anubis) and sooty mangabeys (Cercocebus atys), to test hypotheses about the endocrine regulation of species size differences. First, we expect that levels of hormones and binding proteins predict size change during ontogeny in both species. Second, a high level of integration among the hormones and binding proteins analyzed is expected, with the implication that they act in combination to influence the development of body size and shape. Utilizing a mixed longitudinal sample, we compare change in 18 different measurements, which reflect overall size growth as well as growth in length and circumference, with levels of six growth-related hormones and binding proteins. We examine the relationship between hormone and binding protein levels and morphometrics, using multivariate analyses and "arithmetically-estimated" velocity curves of hormones, binding proteins, to characterize how the endocrine factors analyzed relate to growth. Results suggest that levels of these endocrine factors can be used to predict local and overall growth during ontogeny and that integration between multiple hormone axes is indicated. While important for growth in both species, ontogenetic changes in hormone and binding protein levels are more tightly correlated with changes in morphometric measurements in baboons than mangabeys. These results have important implications for understanding why some smaller-bodied species have higher absolute growth-related hormone levels than larger-bodied species.     

Affiliative behavior of adult female sooty mangabeys (Cercocebus atys)

A 14-month study of 30 adult female members of a captive group of sooty mangabeys investigated their affiliative interactions with group members of varying age and sex. The adult females preferentially affiliated with other adults and interacted less than expected with immature group members. Dyadic frequencies suggested especially frequent affiliation with the three resident adult males, although the pattern of interaction with each male was distinct and apparently was related to age and dominance status of the males. Females of the alpha matriline showed significantly greater affiliation with the males than did those of other matrilines, but this preference was not reciprocated by the males. A preference for grooming older group members (some of the matriarchs and the oldest adult male) was also suggested. In consideration of the taxonomic distinctness of the sooty mangabey from the gray-cheeked mangabey, comparison of these results with those available for albigena were made. Few differences were apparent. Comparisons with the affiliative behavior of Papio females also suggested limited differences, despite the apparently isolated position of the sooty mangabey within the tribe Papionini.     

Female sooty mangabeys (Cercocebus torquatus atys) respond differently to males depending on the male's residence status-preliminary data

I tested the hypothesis that free-ranging female mangabeys (Cercocebus torquatus atys) differentiate between males depending on their residence status. Adult males in this species employ two group-membership strategies: they are either full-time residents or part-time residents (i.e., present for several weeks at a time, then gone for several weeks, then present again, etc.). In a playback experiment I tested whether adult females with young infants responded differently to calls of adult males that were group members during the previous mating season as compared to males that belonged to neighboring groups during the mating season or were complete strangers. Males whose calls were played were present residents, part-time residents (absent for at least 3 months), neighbors, or complete strangers. Because infanticide is a potential risk in mangabeys, I predicted that females would respond differently to males that had resided in the group when their infant was conceived than they would to those that had not been present. The females showed a clear difference in their reaction to the playbacks of vocalizations from resident and part-time resident males as opposed to nonresidents.     

Reproductive parameters and life-history variables in captive golden-bellied mangabeys (Cercocebus agilis chrysogaster)

An understanding of the reproductive physiology of captive primates is vital for their successful management. We report on reproductive parameters and life-history variables collected at the Sacramento Zoo for five female golden-bellied mangabeys (Cercocebus agilis chrysogaster) over a 7-year period. For each female, we collected data on their sexual skins, menses, gestation, and other pregnancy-related factors, such as postconception bleeding and swelling. We used these data to estimate life-history variables, such as age at onset of estrus, menses, and conception, as well as the duration of intervals between births, and between parturition and the resumption of cycling. Cercocebus agilis chrysogaster is comparable to other Cercocebus species in terms of reproductive parameters, although variability is exhibited within and among female subjects. In some cases, it appears that stressful incidents altered cycle length or halted cycling altogether. We suggest the use of husbandry practices that include consistent data collection to enhance regularity in reproductive cycles, and maximize captive breeding success for this rare species.     

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.     

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.     

Application of fecal steroid techniques to the reproductive endocrinology of female verreaux's Sifaka (Propithecus verreauxi)

Solid phase extraction, high performance liquid chromatography, and radioimmunoassay were used to test the validity of fecal steroid analysis for assessing ovarian function in sifaka (Propithecus verreauxi). Daily fecal samples were collected over a 4 month period from two cycling female sifaka, and single samples were collected from females during normal gestation and males while housed at the Duke University Primate Center. Tests of radioimmunoassay validity indicated that solid phase extraction and microradioimmunoassay techniques were reliable and accurate methods for quantifying ovarian steroids in sifaka feces. The progesterone (P₄) antibody specifically quantitated only P₄, while several estrogen metabolites made small contributions to immunoreactive measures of estradiol (E₂). A 1:10 dilution reduced these contributions to 3–15% of the estimated E₂ concentration. Although the spectral data suggested that E₂ was not the major metabolite present, it accounted for the majority of the immunoreactivity at normal assay dilutions. Fecal profiles of immunoreactive E₂ and P₄ in the conceptive female resembled serum profiles of other strepsirhines. E₂ and P₄ were elevated at the end of the conceptive cycle and were more markedly increased in late pregnancy in the two pregnant females. Mating behavior and indices of sexual interest were observed in conjunction with E₂ peaks, although not all peaks were accompanied by observations of sexual behavior. © 1995 Wiley-Liss, Inc.     

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.     

Dietary variation and food hardness in sooty mangabeys (Cercocebus atys): Implications for fallback foods and dental adaptation

We present information on food hardness and monthly dietary changes in female sooty mangabeys (Cercocebus atys) in Tai Forest, Ivory Coast to reassess the hypothesis that thick molar enamel is parsimoniously interpreted as a response to consumption of hard foods during fallback periods. We demonstrate that the diet of sooty mangabeys varies seasonally, but that one food—Sacoglottis gabonensis—is the most frequently consumed food every month and year round. This food is the hardest item in the sooty diet. Given that this species has among the thickest enamel within the primate order, a plausible conclusion is that thick enamel in this taxon evolved not in response to seasonally critical function or fallback foods, but rather to the habitual, year round processing of a mechanically protected foodstuff. These data serve as a caution against de rigueur interpretations that reliance on fallback foods during lean periods primarily explains the evolution of thick enamel in primates. Am J Phys Anthropol 154:413–423, 2014. © 2014 Wiley Periodicals, Inc.     

Sex differences in the vocal repertoire of adult red‐capped mangabeys (Cercocebus torquatus): a multi‐level acoustic analysis

Sex differences in the vocal behavior of nonhuman primates can take various forms: sex‐specific call types, differential production of shared call types, or sex discrepancy in phonation. Also, a growing literature is evidencing that systematically analyzing the vocal repertoires of primates at the call level might lead to underestimating their communicative abilities. Here, we present an extensive multi‐level analysis of the still unknown vocal repertoire of adult red‐capped mangabeys (Cercocebus torquatus), with a special emphasis on sex differences. We collected recordings from seven adult males and seven adult females housed in captivity. We present a structurally‐based classification of mangabey calls that we cross‐validated by an analysis of the associated contexts of emission. We found 12 sound units (including six sex‐specific) that were concatenated to form eight call types (including four sex‐specific), which were produced either singularly or in sequences composed of one (“repetition”) or several (“combination”) call types. We extracted organizational principles that ruled call composition and calling patterns. This revealed a high degree of potentially meaningful variability in terms of semantics and syntax. Male–female discrepancy in terms of phonation could be related to morphological dimorphism and would enable listeners to behave appropriately according to the sex of the caller. Sex differences in repertoire size, structural gradation, and call usage could reflect specificities of male–female social roles. We discuss the pertinence of these sex differences according to social system and habitat quality. Am. J. Primatol. 72:360–375, 2010. © 2010 Wiley‐Liss, Inc.