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.     

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 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.     

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.     

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.     

Information content of sexual swellings and fecal steroids in sooty mangabeys (Cercocebus torquatus atys)

The accuracy and precision of sexual swellings and fecal steroids as measures of ovarian function and the periovulatory period were compared in 4 sexually mature, individually housed, sooty mangabey females. Fecal samples were collected daily over a 10-week period during the normal breeding season. Serum was collected 3×/week, daily during peak swelling, and sex skin was rated 5×/week on a 0–5 relative scale. Both fecal estradiol (fE₂) and progesterone (fP₄) were significantly correlated with serum values in composite E₂-aligned profiles and within the cycles of individual females with average correlations of r_s = 0.6. Follicular phase means for fE₂ and luteal phase means for fP₄ were significantly correlated with the serum means across cycles, suggesting that fecal concentrations could be used to accurately evaluate cycle phases within and across females. In contrast, the timing of peak swelling relative to the periovulatory period varied considerably across the cycles of individual females. Although maximum tumescence appears to bracket the periovulatory period, individual differences in the duration of peak swelling and the timing of its onset and end tend to obscure the exact time of ovulation in relation to maximal tumescence. These data illustrate the utility of fecal steroid analysis as a tool for further evaluation of the signal value of sexual skin and its role in mating interactions. © 1996 Wiley-Liss, Inc.     

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.     

Clinicopathologic Characteristics,Prevalence, and Risk Factors of Spontaneous Diabetes in Sooty Mangabeys (Cercocebus atys)

In 2008, clinical observations in our colony of sooty mangabeys (Cercocebus atys) suggested a high frequency of type 2 diabetes. Postmortem studies of diabetic animals revealed dense amyloid deposits in pancreatic islets. To investigate these findings, we screened our colony (97 male mangabeys; 99 female mangabeys) for the disease from 2008 to 2012. The overall prevalence of diabetes was 11% and of prediabetes was 7%, which is nearly double that reported for other primate species (less than 6%). Fructosamine and triglyceride levels were the best indicators of diabetes; total cholesterol and glycated hemoglobin were not associated with disease. Increasing age was a significant risk factor: prevalence increased from 0% in infants, juveniles, and young adults to 11% in adults and 19% in geriatric mangabeys. Sex, medroxyprogesterone acetate exposure, and SIV status were unrelated to disease. Weight was marginally higher in prediabetics, but body condition did not indicate obesity. Of the 49 mangabeys that were necropsied after clinical euthanasia or death from natural causes, 22 were diabetic; all 22 animals demonstrated pancreatic amyloid, and most had more than 75% of islets replaced with amyloid. We conclude that type 2 diabetes is more common in mangabeys than in other primate species. Diabetes in mangabeys has some unusual pathologic characteristics, including the absence of altered cholesterol levels and glycated hemoglobin but a robust association of pancreatic insular amyloidosis with clinical diabetes. Future research will examine the genetic basis of mangabey diabetes and evaluate additional diagnostic tools using imaging and serum markers.Abbreviations: HbA1c, glycated hemoglobin; MPA, medroxyprogesterone acetate; YNPRC, Yerkes National Primate Research CenterSooty mangabeys (Cercocebus atys) are Old World NHP that are native to West Africa. Historically their use in research has been limited to infectious disease studies, leprosy studies, and behavioral research.^14,25 Over the past 20 to 30 y, they have been used in HIV–AIDS research. Mangabeys are natural hosts of SIV_smm, which is recognized as the origin of HIV2 infection in humans.^7,8,30,36,42 SIV typically is nonpathogenic in mangabeys despite high levels of virus replication, which makes this species a unique and invaluable model in AIDS research.^7,30,36,42 Our facility maintains a colony of approximately 200 sooty mangabeys. In 2008 clinical observations of relative hyperglycemia, glucosuria, and weight loss in our colony suggested that type 2 diabetes mellitus occurred at a relatively high frequency in this population. Spontaneous diabetes was found in 10% of the colony, and 5% of animals were prediabetic; this incidence is higher than that typically reported for other NHP species, such as cynomolgus macaques (less than 1% to 2%)²² and chimpanzees (less than 1%).³⁷ The prevalence of spontaneous diabetes in humans is typically 8.3%.^2,6,22,37 In addition, necropsies revealed that many affected animals had dense amyloid deposits in pancreatic islet cells. Insular amyloidosis was seen on histology, with a total replacement of islets by amyloid deposition in advanced diabetes. Advanced diabetes was determined by increased weight loss and severity of relative hyperglycemia. The increased clinical prevalence of diabetes in our mangabey colony prompted additional characterization of the clinicopathologic profile, risk factors, and prevalence of diabetes in our mangabey colony.The form of diabetes in this mangabey colony is characterized as type 2 diabetes mellitus, as they have hyperglycemia, hypertriglyceridemia, and islet amyloidosis. Type 2 diabetes mellitus is the most common of the 3 forms of diabetes, and has been documented in humans and NHP,^22,31,37,55 including rhesus macaques (Macaca mulatta), cynomolgus macaques (Macaca fascicularis), Celebes crested macaques (Macaca nigra), bonnet macaques (Macaca radiate), pigtailed macaques (Macaca nemestrina), vervet monkeys (Chlorocebus pygerythrus), squirrel monkeys (Saimiri sciureus), chimpanzees (Pan troglodytes), and woolly monkeys (Lagothrix spp.).^{1,24,31,52,55} Type 2 diabetes is a chronic metabolic disorder in which insulin resistance occurs in liver, muscle, and adipose tissue. As type 2 diabetes progresses, it also can be characterized as a relative insulin deficiency.^{1,6,15,22,29,31,37,55} The initial clinical presentation of diabetes in humans and NHP includes polydipsia, polyuria, polyphagia, weight loss, and lethargy.^{1,6,22,27,31,37,55} Similar presentation was observed in our colony of diabetic mangabeys.Diagnostic criteria of diabetes in NHP species is similar to that for humans and is based on clinical symptoms and routine lab tests, including serum chemistry panel to evaluate persistent fasting hyperglycemia, hypertriglyceridemia, and hypercholesterolemia.^{2,6,11,16-18,21,22,29,31,37,48-50,52,55} Hypertriglyceridemia and hypercholesterolemia frequently are elevated due to diabetes and therefore are used as supportive diagnostic markers. In addition, the disease is characterized by transient hyperinsulinemia followed by insulin deficiency subsequent to glucose challenge. Urinalysis is used to evaluate glucosuria and ketonuria. These tests are not exclusive for diagnosing diabetes and can be inconsistent between species, thus making conclusive diagnosis challenging. For example, hyperglycemia can be a transient finding associated with recent food intake or stress associated with restraint for blood sample collection or anesthetic access, whereas hypertriglyceridemia can be seen in obese animals and those with other metabolic diseases such as pancreatitis and hypothyroidism.^1,22,37,55The typical clinical approach to the diagnosis of diabetes in NHP and other veterinary patients includes evaluation of fructosamine and glycated hemoglobin (HbA1c) levels and glucose tolerance testing. These tests are indices of glycemic control and are used in clinical settings primarily to assess prognosis and response to treatment; they are also useful for the initial diagnosis of diabetes when used in parallel with serum chemistry markers. Fructosamine and HbA1c can both provide information on long-term glycemic control, because fructosamine reflects average blood glucose levels over 2 to 3 wk whereas HbA1c reflects average blood glucose over 2 to 3 mo preceding blood collection. HbA1c is the primary test for diabetes in human medicine,^6,31,35,37 whereas fructosamine is commonly used in veterinary medicine. Glucose tolerance testing provides an indirect measure of insulin sensitivity, but it is not frequently used clinically in NHP because of the requirement for prolonged physical restraint or sedation.^{1,21,22,26,27,34,37,55}Prevention and management of diabetes in NHP and humans can be achieved by identifying potential risk factors, including age, weight, sex, genetics, hormone drug exposure, and viral status.^{1,6,15,22,29,31,37,42,55} Advanced age, obesity, sex, and genetics are associated with diabetes in some species of NHP and humans.^{1,6,15,22,29,31,37,55} In addition, exposure to drugs such as medroxyprogesterone acetate (MPA) is suspected to be linked to diabetes due to the hormonal effects of progesterone impacting glucoregulatory function.^{1,6,10,22,23,31,34,55} MPA exposure is of interest, because it is used regularly in our mangabey colony as both a contraceptive and as therapy for endometriosis. In addition, SIV status is being evaluated as a risk factor, because a portion of our colony is SIV positive. Although HIV is not thought to be associated with diabetes in people, SIV pathogenesis in mangabeys differs; therefore it was of interest to explore the possible association of SIV and diabetes in mangabeys.^7,30,36,42 Pancreatic insular amyloidosis has been documented to be associated with type 2 diabetes in several species. Amyloidosis is a group of disorders that are caused by extracellular deposition of misfolded proteins that can result in impaired function of any organ.^{15,20,23,28,32,43,45,48,49} Because a high incidence of pancreatic insular amyloid was noted at necropsy, we sought to document the relationship with clinical diabetes in mangabeys.Spontaneous type 2 diabetes mellitus has been well documented in several species of NHP. Because the literature contains little information regarding the clinicopathologic features (the ‘profile’), risk factors, and prevalence of spontaneous diabetes mellitus in sooty mangabeys, the primary aims of the current study were 1) to determine whether elevated levels of fasting blood glucose, fructosamine, HbA1c, triglycerides, and total cholesterol levels are reliable diagnostic markers of type 2 diabetes mellitus in this NHP species; 2) to determine whether age, sex, MPA exposure, and SIV status influence the risk of diabetes; 3) to determine whether body weight influences diabetic status; 4) to evaluate the relationship between pancreatic amyloidosis and diabetes mellitus; and 5) to characterize the prevalence of diabetes mellitus in the mangabey population at our institution. To our knowledge, this report is the first to describe the natural occurrence of type 2 diabetes mellitus within a captive colony of sooty mangabeys. We hypothesized that blood glucose, fructosamine, HbA1c, triglyceride, and total cholesterol would be reliable diagnostic markers and that age, sex, and MPA exposure would influence the risk of diabetes in this species.     

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.     

Hematology and serum chemistry in the white-crowned mangabey (Cercocebus torquatus lunulatus) and in the mandrill (Mandrillus sphinx)

Abstract: Reference values of some hematologic and plasma chemical parameters were established in two species of clinically normal Cercopithecidae. The following variables were studied in seven mandrills (Mandrillus sphinx) and nine white-crowned mangabeys (Cercocebus torquatus lunulatus): hematocrit, hemoglobin concentration, erythrocyte and leucocyte counts, mean corpuscular volume, mean corpuscular hemoglobin, mean corpuscular hemoglobin concentration, glucose, urea, uric acid, cholesterol, creatinine, aspartate aminotransferase, alanine aminotransferase, alkaline phosphatase, creatinine phosphokinase, lactic dehydrogenase, gamma glutamyl transpeptidase, total serum proteins, albumin, globulins, albumin-globulin ratio, sodium, potassium, calcium, magnesium, total phosphorus, chloride, and serum osmolality. Few differences were observed when compared with human hematological data and with other species of Cercopithecidae Primates.     

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.     

Social compatibility in a newly formed all‐male group of white crowned mangabeys (Cercocebus atys lunulatus)

Surplus males in primate captive populations are a common problem for zoos. Some captive breeding programs promote all‐male groups as an adequate option to house surplus males, but there have been few attempts to assess the feasibility of this management technique across primate species. The present study provides preliminary data regarding social compatibility within a newly formed all‐male group of four white crowned mangabeys (Cercocebus atys lunulatus). The study was conducted at the Valencia Zoo (Spain), where data on social behavior were collected over 6 months using continuous focal animal sampling for a total of 87 hr of observation. Results show that low intensity aggressive behaviors (facial threats) were expressed at high rates, whereas physical aggression (fights) rarely occurred. Aggression was more frequent among individuals belonging to the same age–gender class. Regarding affiliative behaviors, every individual actively sought proximity to all other group members through positive approaches, and although not all males carried out social grooming, every male was groomed by at least one group member. Our results suggest that the group was compatible socially because social relationships among the individuals were not neutral, and physical aggression occurred at low rates. The present study provides preliminary data supporting the feasibility of all‐male groups as a management option for surplus males in captive populations of white crowned mangabeys. Nevertheless, further studies are needed to be able to generalize both within and across species. Zoo Biol 0:1–7, 2007. © 2006 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.     

Links between habitat degradation,and social group size,ranging, fecundity,and parasite prevalence in the Tana River mangabey (Cercocebus galeritus)

We investigated the effects of anthropogenic habitat degradation on group size, ranging, fecundity, and parasite dynamics in four groups of the Tana River mangabey (Cercocebus galeritus). Two groups occupied a forest disturbed by human activities, while the other two occupied a forest with no human disturbance. We predicted that the groups in the disturbed forest would be smaller, travel longer distances daily, and have larger home ranges due to low food tree abundance. Consequently, these groups would have lower fecundity and higher parasite prevalence and richness (number of parasite species). We measured the abundance of food trees and anthropogenic activity in the forests, the groups' daily travel distances and home range sizes, and censused social groups over 12 months. We also analyzed fecal samples for gastrointestinal parasites from three of the groups. The disturbed forest had a lower abundance of food trees, and groups in this forest traveled longer distances, had larger home range sizes, were smaller, and had lower fecundity. The groups in the disturbed forest had higher, although not statistically significant, parasite prevalence and richness. This study contributes to a better understanding of how anthropogenic habitat change influences fecundity and parasite infections in primates. Our results also emphasize the strong influence of habitat quality in determining daily travel distance and home range size in primates. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.