Developmental variables and dominance rank in adolescent male mandrills (Mandrillus sphinx).

Previous research on semifree-ranging mandrills has shown that the degree of secondary sexual development differs among adult males. While some males are social, brightly colored, and have large testes and high levels of plasma testosterone, other males are peripheral or solitary, and lack fully developed secondary sexual features. In order to determine how these differences among males arise, and to investigate the influence of social factors, we examined the adolescent development of 13 semifree-ranging male mandrills of known age. Testicular volume began to increase markedly at 5.5 yr, and males began to develop secondary sexual adornments at the age of 6 yr. Males attained adult size and secondary sexual development at an average age of 9 yr. As males developed, they peripheralized, decreasing from 100% group-associated at 5 yr to 20% at 8 yr. At 9 yr some males reentered the social group and attained alpha rank, while others remained peripheral or solitary. Within this average development, there was marked variation among males in the timing of development. Adolescent males that were dominant for their age had higher testosterone levels, larger testes, and more advanced secondary sexual development than subordinate males. The implications of these findings are discussed in the light of differences that occur among adult males, male-male competition, and the evolution of secondary sexual adornments in this species.     

Circannual changes in the secondary sexual adornments of semifree-ranging male and female mandrills (Mandrillus sphinx)

Male mandrills (Mandrillus sphinx) have spectacular secondary sexual adornments. These include red and blue sexual skin on the face, rump, and genitalia; a sternal scent-marking gland; and a "fatted" rump. Mandrills are seasonal breeders, and in other seasonally-breeding primate species members of both sexes may show increased expression of secondary sexual characteristics during the mating season. We examined changes in male secondary sexual adornments and testosterone levels, in relation to seasonal changes in the female reproductive cycle and sexual skin morphology, in two semifree-ranging mandrill groups. Females showed circannual changes in sexual skin tumescence, and periods of tumescence peaked from May-July in a long-established group. However, formation of a second, smaller group, two years previous to commencement of the study, disrupted the seasonal pattern of sexual skin tumescence and births. As the groups occupied adjacent enclosures, it appears that social factors, as well as physical environment, affected the seasonal patterning of reproduction in females. Male mandrills, by contrast, did not exhibit marked circannual changes in secondary sexual traits. Although adult male testicular volume and circulating testosterone levels increased significantly during the mating season, sexual skin coloration and rump "fattedness" showed no consistent changes with season. There was some evidence to suggest that maturing males (ages 5-8 yr) showed increased development of red sexual skin during mating periods, but once males had fully developed secondary sexual adornments, they remained stable throughout the year. The possible reasons for this are discussed in relation to intermale competition and social organization in mandrills.     

Factors affecting fecal glucocorticoid levels in semi-free-ranging female mandrills (Mandrillus sphinx)

Subordinate female cercopithecine primates often experience decreased reproductive success in comparison with high-ranking females, with a later age at sexual maturity and first reproduction and/or longer interbirth intervals. One explanation that has traditionally been advanced to explain this is high levels of chronic social stress in subordinates, resulting from agonistic and aggressive interactions and leading to higher basal levels of glucocorticoids. We assessed the relationships among fecal cortisol levels and reproductive condition, dominance rank, degree of social support, and fertility in female mandrills (Mandrillus sphinx) living in a semi-free-ranging colony in Franceville, Gabon. Lower-ranking females in this colony have a reproductive disadvantage relative to higher-ranking females, and we were interested in determining whether this relationship between dominance rank and reproductive success is mediated through stress hormones. We analyzed 340 fecal samples from 19 females, collected over a 14-month period. We found that pregnant females experienced higher fecal cortisol levels than cycling or lactating females. This is similar to results for other primate species and is likely owing to increased metabolic demands and interactions between the hypothalamus-pituitary-adrenal axis, estrogen, and placental production of corticotrophin releasing hormones during pregnancy. There was no influence of dominance rank on fecal cortisol levels, suggesting that subordinate females do not suffer chronic stress. This may be because female mandrills have a stable social hierarchy, with low levels of aggression and high social support. However, we found no relationship between matriline size, as a measure of social support, and fecal cortisol levels. Subordinates may be able to avoid aggression from dominants in the large enclosure or may react only transiently to specific aggressive events, rather than continuously expecting them. Finally, we found no relationship between fecal cortisol levels and fertility. There was no difference in fecal cortisol levels between conceptive and nonconceptive cycles, and no significant relationship between fecal cortisol level and either the length of postpartum amenorrhea or the number of cycles before conception. This suggests that the influence of dominance rank on female reproductive success in this population is not mediated through chronic stress in subordinate females, and that alternative explanations of the relationship between social rank and reproduction should be sought.     

Social and seasonal influences on the reproductive cycle in female mandrills (Mandrillus sphinx)

We present 12 years of perineal swelling data for a semifree-ranging colony of mandrills (Mandrillus sphinx), and evaluate the influence of rank, parity, and seasonality on reproductive parameters. Female sexual swellings showed a seasonal pattern, with August the median month of ovulation. Overlapping periovulatory periods did not decrease the likelihood of conception. Females showed their first genital swelling at age 3.6 years (n = 28; range, 3.2-4.6 years), and higher-ranking females experienced their first swelling earlier than low-ranking females. Median postpartum amenorrhea (PPA) duration was 208 days (n = 92; range, 74-538 days). PPA was longer in primiparous females than in multiparous females, but PPA duration was unrelated to female rank. Median follicular phase duration was 24 days for the first cycle after parturition (n = 84; range, 12-40 days), shortening to 17 days in subsequent cycles (n = 55; range, 6-39 days). The follicular phase was longer in nulliparous females than in parous females, but was unrelated to female rank. Median cycle length (from one sexual swelling breakdown to the next) was 38 days (n = 57; range, 18-108 days). Eighty-seven percent of conceptions occurred within two cycles, and half of the nulliparous females conceived during their first swelling cycle. Lower-ranking females were more likely to require more cycles to conceive than higher-ranking females. The cycling phase was significantly longer in nulliparous females than in parous females, and was also significantly longer in lower-ranking females than in higher-ranking females. We discuss the influence of provisioning on female reproductive parameters, the influence of parity and rank on the different phases of the interbirth interval, and the evolution of long and variable follicular phases in mandrills.     

Changes in the secondary sexual adornments of male mandrills (Mandrillus sphinx) are associated with gain and loss of alpha status

Two semifree-ranging mandrill groups, inhabiting large, naturally rainforested enclosures in Gabon, were studied to measure morphological, endocrine, and behavioral changes that occurred when adult males rose, or fell, in dominance rank. Gaining alpha rank (N = 4 males) resulted in increased testicular size and circulating testosterone, reddening of the sexual skin on the face and genitalia, and heightened secretion from the sternal cutaneous gland. Blue sexual skin coloration was unaffected. New alpha males increased in rump "fattedness," but not in body mass, and spent more time associated with other group members, rather than ranging alone. Loss of alpha position (N = 4 males) resulted in less pronounced effects than those that occurred after males had risen to alpha positions. Deposed alpha males showed decreased testicular volume, decreased body mass, a reduction in the extent of red (but not blue) sexual skin coloration, and decreased sternal gland activity. Deposed males did not decrease in the brightness of sex skin coloration. These results demonstrate that male-male competition and rank reversals have remarkable effects upon testicular function, secondary sexual traits, and behavior in the adult male mandrill. Secondary sexual traits respond to changes in male social status and therefore may be important as intrasexual signals of dominance rank.     

Canine tooth size and fitness in male mandrills (Mandrillus sphinx)

Sexual selection theory explains the evolution of exaggerated male morphologies and weaponry, but the fitness consequences of developmental and age-related changes in these features remain poorly understood. This long-term study of mandrill monkeys (Mandrillus sphinx) demonstrates how age-related changes in canine tooth weaponry and adult canine size correlate closely with male lifetime reproductive success. Combining long-term demographic and morphometric data reveals that male fitness covaries simply and directly with canine ontogeny, adult maximum size, and wear. However, fitness is largely independent of other somatometrics. Male mandrills sire offspring almost exclusively when their canines exceed approximately 30 mm, or two-thirds of average adult value (45 mm). Moreover, sires have larger canines than nonsires. The tooth diminishes through wear as animals age, corresponding with, and perhaps influencing, reproductive senescence. These factors combine to constrain male reproductive opportunities to a brief timespan, defined by the period of maximum canine length. Sexually-selected weaponry, especially when it is nonrenewable like the primate canine tooth, is intimately tied to the male life course. Our analyses of this extremely dimorphic species indicate that sexual selection is closely intertwined with growth, development, and aging, pointing to new directions for sexual selection theory. Moreover, the primate canine tooth has potential as a simple mammalian system for testing genetically-based models of aging. Finally, the tooth may record details of life histories in fossil primates, especially when sexual selection has played a role in the evolution of dimorphism.     

Changes in social interactions during adolescence in male mandrills (Mandrillus sphinx)

The adolescent period in male mandrills extends from the time the testicles descend (at the age of 3-4 years) to the time adult characteristics develop (at the age of 10 years), and is thus one of the longest adolescent periods in cercopithecines. In this short cross-sectional study of 11 male mandrills (4.7-9.1 years old), we analyzed social behavioral patterns to investigate partner preference and changes in types of interactions throughout puberty. The mandrills were separated into two clusters on the basis of all of the social interactions scored, as well as the age and sex of the protagonist. During early to mid puberty, immature individuals interacted preferentially with other male adolescents and juveniles. Playing was an important activity, and some affiliative interactions with juveniles were observed. Older adolescents interacted more with adult males and females. These older adolescents were predominantly aggressive toward other adolescents, females, and juveniles, and showed little or no affiliative or playful behaviors. These results indicate a shift in social partners: older males interacted more frequently with adult males, and their behavior involved more aggression and less submission compared to younger adolescents, which showed predominantly submissive and playful behavior. These changes are consistent with preparation for dispersal and future intermale competition.     

Sexual swelling in mandrills (Mandrillus sphinx): a test of the reliable indicator hypothesis

Various hypotheses have been proposed to account for the functionof sexual swellings in female primates, but few empirical dataexist to test predictions arising from these hypotheses. Controversyhas recently arisen over a field study that appeared to supportthe predictions of the reliable indicator hypothesis. This hypothesisproposes that females compete for males or matings, that differencesin swelling size between females reliably advertise female quality,and that males use swelling characteristics to differentiallyallocate mating effort to females with certain swelling characteristics,hence to females of higher quality. To provide an independenttest of this hypothesis, we collected data concerning the sizeand coloration of 40 sexual swellings for 29 semi-free-rangingfemale mandrills, varying in age and parity, along with dataconcerning the behavior of males toward the females, and comparedthese with the long-term reproductive history of the females.We examined the following predictions: (1) swelling characteristicsare consistent across subsequent cycles for individual females,(2) swelling characteristics indicate aspects of female reproductivequality, and (3) males prefer to mate with females that showparticular swelling characteristics. Our results support prediction1; we found little change in swelling characteristics acrossswellings for individual females. However, we found no significantrelationships between female reproductive history and swellingcharacteristics and, thus, no support for prediction 2. Finally,we found only limited support for prediction 3; females withlarger (wider) sexual swellings were more likely to have a spermplug when maximally swollen. However, male mate-guarding wasnot significantly related to female swelling characteristics.Furthermore, in situations in which more than one female wasmaximally swollen, the alpha male (who has "free" choice) didnot show the most interest in the female with the largest swelling.We conclude that the reliable indicator hypothesis does notexplain variation in sexual swellings in female mandrills.     

Constraints on control: factors influencing reproductive success in male mandrills (Mandrillus sphinx)

Over the last decade, paternity analysis using molecular markershas revealed that observed mating systems do not necessarilycorrelate with reproductive systems and thus cannot providereliable information about male reproductive success (RS). Thisis especially true for primate species with a complex multimale-multifemalesocial organization, such as mandrills (Mandrillus sphinx).Using molecular markers for the measurement of individual RSand a comprehensive data set comprising 193 offspring from 27birth cohorts over a 20-year period of sampling, we investigatedthe social, genetic, and demographic factors that may influencethe probability of paternity by dominant male mandrills, livingin a semi–free-ranging colony. We observed a significantskew in RS towards dominant males, with their probability ofpaternity increasing as the number of adult males in the groupincreased, and when they were closely related to subordinateadolescent males. Conversely, the probability of dominant malessiring infants decreased when the number of simultaneously tumescentfemales increased. Fewer offspring were sired by dominant maleswhen female partners were closely related to them and when therelatedness between dominant and subordinate adult males increased.These two last points suggests particularly that mechanismsof kin recognition are operating to avoid the costs of inbreedingand may also reflect the lower costs to dominant males of losingconception opportunities to more closely related subordinateadult males. This study is, to our knowledge, one of the firstin primates to use an integrative approach and multivariateanalysis to show that multiple factors are involved in determiningthe probability of paternity by dominant males.     

Life history in male mandrills (Mandrillus sphinx): physical development, dominance rank, and group association

We assess life history from birth to death in male mandrills (Mandrillus sphinx) living in a semifree-ranging colony in Gabon, using data collected for 82 males that attained at least the age of puberty, including 33 that reached adulthood and 25 that died, yielding data for their entire lifespan. We describe patterns of mortality and injuries, dominance rank, group association, growth and stature, and secondary sexual character expression across the male lifespan. We examine relationships among these variables and investigate potential influences on male life history, including differences in the social environment (maternal rank and group demography) and early development, with the aim of identifying characteristics of successful males. Sons of higher-ranking females were more likely to survive to adulthood than sons of low-ranking females. Adolescent males varied consistently in the rate at which they developed, and this variation was related to a male's own dominance rank. Males with fewer peers and sons of higher-ranking and heavier mothers also matured faster. However, maternal variables were not significantly related to dominance rank during adolescence, the age at which males attained adult dominance rank, or whether a male became alpha male. Among adult males, behavior and morphological development were related to a male's own dominance rank, and sons of high-ranking females were larger than sons of low-ranking females. Alpha males were always the most social, and the most brightly colored males, but were not necessarily the largest males present. Finally, alpha male tenure was related to group demography, with larger numbers of rival adult males and maturing adolescent males reducing the time a male spent as alpha male. Tenure did not appear to be related to characteristics of the alpha male himself.     

Preliminary report on the grouping of mandrills (Mandrillus sphinx) in Cameroon

A field study of mandrill was carried out from 1979 to 1983 in Cameroon for 27 months. Group size of mandrills ranged from 15 to 95 and composition was estimated by direct and indirect observations. The ratio of group size to one adult male was 13.9, larger than other baboon species except the drill. Solitary males were seen. The mandrill may have two types of groups: one-male and multi-male. The multi-male group was observed to split into subgroups, one of which was sometimes a one-male group. The multi-male subgroup was assumed to be composed of several one-male groups. The home range area of mandrills was estimated to be at least 5 km⁵ to 28 km². Their large home range size could be related to their characteristic feeding pattern in the forest.     

Life history correlates of inbreeding depression in mandrills (Mandrillus sphinx)

Inbreeding depression reflects the negative consequences of increased homozygosity at genes that affect fitness. We investigate inbreeding depression in a semi-free-ranging colony of mandrills (Mandrillus sphinx), using high-quality pedigree data, comprising five maternal generations and 20 years of morphological and demographic data. We examine the relationship between inbreeding coefficients and four fitness correlates: two growth parameters (mass and height for age) and longevity in both sexes, and age at first conception in females. Inbreeding was correlated with both growth parameters, but only in females, with inbred females being smaller than noninbred females. Inbreeding was also correlated significantly with age at first conception, with inbred females giving birth earlier in life than noninbred females. We suggest that sex-biased maternal investment may explain this sex-differential response to inbreeding, although the lack of a significant association between inbreeding and growth in males may also be due to the provisioned nature of the colony. The surprising relationship between age at first conception and inbreeding may be related to smaller adult size in inbred females, or to their being less able to escape from male sexual coercion.     

Growth and ontogeny of sexual size dimorphism in the mandrill (Mandrillus sphinx)

We present body mass (N = 419) and crown-rump length (CRL, N = 210) measurements from 38 male and 49 female mandrills born into a semifree-ranging colony in order to describe growth from birth to adulthood, and to investigate maternal influences upon growth. Adult male mandrills are 3.4 times the body mass, and 1.3 times the CRL, of adult females. Body mass dimorphism arises from a combination of sex differences in length of the growth period (females attain adult body mass at 7 years, males at 10 years) and growth rate. Both sexes undergo a subadult growth spurt in body mass, and this is much more dramatic in males (peak velocity 551 g/months +/- 89 SEM at 84-96 months). CRL dimorphism arises from bimaturism (females attain adult CRL at 6 years, males after 10 years), and neither sex shows a particular subadult growth spurt in CRL. Sexual size dimorphism thus represents important time and metabolic costs to males, who mature physically approximately 3-4 years after females. Considerable interindividual variation occurs in the size-for-age of both sexes, which is related to maternal variables. Older mothers have heavier offspring than do younger mothers, and higher-ranking mothers have heavier offspring than do lower ranking mothers. Mass advantages conferred upon offspring during lactation by older and higher-ranking mothers tend to persist postweaning in both sexes. Thus maternal factors affect reproductive success in both sexes, influencing the age at which offspring mature and begin their reproductive career.     

Development from birth to sexual maturity in a semi-free-ranging colony of mandrills (Mandrillus sphinx) in Gabon.

This report presents information collected over 7 years (1983-1990) in Gabon, on a breeding group of 14, increasing to 45, mandrills maintained in a rainforest enclosure. Under these conditions, a seasonal cycle of mating (June-October) and birth (January-May) occurred. Females began to exhibit sexual skin swellings at age 2.75-4.5 years (3.6 +/- 0.6 years, mean +/- SD; n = 10) and first delivered offspring when 3.25-5.5 years old (4.4 +/- 0.8 years; n = 9). Gestation periods ranged from 152 to 176 days (167 +/- 9 days; n = 6 accurately dated pregnancies) and interbirth intervals from 11 to 15 months (12.4 +/- 1.3 months; n = 15). Females could reproduce 2 years before attaining adult body weight (10-15 kg) and complete dental eruption by 5.0-5.5 years. Males, by contrast, developed more slowly, reaching adult body weight (30-35 kg) and testicular volume (volume of left testis: 25-30 ml) at 8 years. Consistently high circulating testosterone concentrations (8.17 +/- 2.0 ng ml-1) could be measured by 9 years of age. Fully developed males exhibited fatting of the rump and flanks, as well as striking sexual skin coloration and an active sternal cutaneous gland; little expression of these features was evident during pubertal development. Marked individual age differences occurred with regard to the onset and complete development of these features, suggesting possible interactions between social environment and physical maturation.     

Feeding ecology of mandrills (Mandrillus sphinx) in campo animal reserve,Cameroon

A field study on the ecology of mandrills (Mandrillus sphinx) was carried out for 28 months in Cameroon. Fresh food remnants and large quantities of fresh feces were collected by following the groups. Analyses of these products indicated that fruit (including seeds), monocotyledonous plant leaves and insects (especially ants and termites), were frequently eaten. Mandrills mostly ate the plant and animal foods in the lower forest stratum and on the ground. Fallen seeds and monocotyledonous plant leaves were eaten more frequently in the minor fruiting season than in the major fruiting season presumably to compensate for the shortage of fresh fruit during the former. Daily travel distances were shorter during the minor fruiting season than during the major fruiting season, because in the minor fruiting season mandrills forage for small food items, such as the new leaves and piths of monocotyledons and fallen seeds which are sparsely distributed on the ground, while in the major fruiting season they search for widely distributed food such as fruit. The daily pattern of group movement and a food intake experiment suggest that mandrills move and feed continuously throughout the day. Use of fallen seeds and monocotyledonous plant leaves appears to enable mandrills to maintain a terrestrial life in the tropical rain forest. The feeding and ranging characteristics of mandrills are basically similar to those of other baboon species in open land, though their environments differ extremely.     

A preliminary investigation of urinary testosterone and cortisol levels in wild male mountain gorillas

Urinary steroid hormone levels were measured in wild male mountain gorillas (Gorilla gorilla beringei) to determine how levels of testosterone and cortisol corresponded with age and social rank. Urine samples were collected noninvasively from 18 males, ranging in age from 3–26 years, in three groups of wild mountain gorillas at the Karisoke Research Center, Rwanda, Africa, and samples were analyzed using radioimmunoassay procedures. Males were classified as being immature (<7 years), maturing (10–13 years), or adult (+13 years of age). Immature males had significantly lower levels of testosterone and higher levels of cortisol than both maturing and adult males. No differences in testosterone or cortisol levels were found between maturing and adult males. Dominant males exhibited a trend toward significantly higher levels of testosterone than subordinate males, but no difference was found between cortisol levels of dominant and subordinate males. These results suggest that the increase in testosterone associated with puberty occurs prior to any outward sign of development of secondary sexual characteristics. Within-group male–male competition may affect testosterone levels, but the lack of difference in cortisol levels between dominant and subordinate males suggests that subordinate males are not socially stressed, at least as measured by cortisol. Am. J. Primatol. 43:51–64, 1997. © 1997 Wiley-Liss, Inc.     

Selective attention toward female secondary sexual color in male rhesus macaques

Pink-to-red anogenital and facial sexual skin occurs in females of many primate species. Since female sexual skin color varies with reproductive state, it has long been assumed that color acts to stimulate male sexual interest. Although there is supportive evidence for this as regards anogenital skin, it is unclear whether this is also the case for facial sexual skin. In this study we experimentally manipulated digital facial and hindquarter images of female rhesus macaques (Macaca mulatta) for color within the natural range of variation. The images were presented to adult male conspecifics to assess whether the males exhibited visual preferences for red vs. non-red female coloration, and whether preferences varied with anatomical region. The males displayed significantly longer gaze durations in response to reddened versions of female hindquarters, but not to reddened versions of faces. This suggests that female facial coloration may serve an alternative purpose to that of attracting males, and that the signal function of sexual skin and the intended recipients may vary across anatomical regions.     

The effects of temporary removal of the alpha male on the behavior of subordinate male vervet monkeys

The effects of temporary removal of the alpha male on the behavior of subordinate adult male vervet monkeys were evaluated. Twelve subordinate males from six captive multimale, multifemale vervet monkey groups were observed in two conditions: when all group members were present and when the alpha male was temporarily removed from each group. In the absence of the alpha male, subordinate males initiated more affiliative behavior and increased the amount of time spent in proximity to females but their rates of aggression were unaltered. Increased affiliative behavior was selectively directed to high-ranking females and their offspring. Under removal conditions, subordinate male behavior did not resemble that of alpha males in intact conditions: they differed in their proximity to and affiliative behavior towards other group members. In the absence of the alpha male, females increased their aggression towards subordinate males. These observations suggest that the presence of alpha males strongly inhibits subordinate males' behavior. When the constraints of the alpha male's presence are removed, subordinate males rapidly engage in behavior that may enhance their likelihood of attaining high rank. In combination with prior studies, the data also indicate that the behaviors involved in the maintenance of high rank by alpha males differ from those subordinates use to acquire dominance. Finally the current study supports the view that aggression by female vervets may be highly influential in determining male ascendency to dominant rank.