Female Mandrills Research Articles

Emotional states following grooming in female mandrills.

Grooming is a common cooperative behavior whose exact costs and benefits are still to be fully elucidated. In this study, we evaluated the emotional consequences of giving and receiving grooming in mandrills (Mandrillus sphinx), and how these may change along time after the termination of grooming. We used scratching as a behavioral indicator of anxiety-like emotions. Groomees showed increased scratching immediately after the termination of grooming, while in the subsequent minutes scratching decreased below baseline. The initial increase was larger after longer grooming events, suggesting it represented a case of postinhibitory rebound. The subsequent decline in scratching rates was larger after grooming received by a kin, suggesting interactions with kin are particularly relaxing. Scratching rates shown by groomers were unaffected by grooming interactions. These results highlight that the emotional states following grooming can have a complex time course, and may contribute to explain the inconsistencies found in the previous literature.

Social and sexual consequences of facial femininity in a non-human primate

In humans, femininity shapes women's interactions with both genders, but its influence on animals remains unknown. Using 10 years of data on a wild primate, we developed an artificial intelligence-based method to estimate facial femininity from naturalistic portraits. Our method explains up to 30% of the variance in perceived femininity in humans, competing with classical methods using standardized pictures taken under laboratory conditions. We then showed that femininity estimated on 95 female mandrills significantly correlated with various socio-sexual behaviors. Unexpectedly, less feminine female mandrills were approached and aggressed more frequently by both sexes and received more male copulations, suggesting a positive valuation of masculinity attributes rather than a perception bias. This study contributes to understand the role of femininity on animal's sociality and offers a framework for non-invasive research on visual communication in behavioral ecology.

Socially bonded females face more sexual coercion in a female-philopatric primate

Sexual coercion is a manifestation of sexual conflict increasing male mating success while inflicting costs to females. Although previous work has examined inter-individual variation in male sexually coercive tactics, little is known about female counter-strategies. We investigated whether social bonding mitigates the extent of sexual coercion faced by female mandrills (Mandrillus sphinx), as a putative mechanism linking sociality to fitness. Surprisingly, females faced the most coercion from those males with whom they formed the strongest bonds, while the strength of a female-male bond was also positively correlated with coercion from all other males. Finally, greater social integration in the female network was positively correlated with coercion, through a direct 'public exposure' mechanism and not mediated by female reproductive success or retaliation potential. Altogether, this study shows that neither between- nor within-sex bonds are protective against sexual coercion and identifies, instead, a hidden cost of social bonding.

Dynamics of intersexual dominance in a highly dimorphic primate

Intersexual dominance, which is measured by the probability that members of one sex elicit submission of members of the other sex during agonistic interactions, is often skewed in favor of males. However, even in sexually dimorphic species, several factors may influence intersexual dominance. Here, we use an 8-year dataset to examine the dynamics of intersexual dominance in wild-living mandrills (Mandrillus sphinx). Mandrills exhibit an extreme male-biased sexual size dimorphism but females show pronounced kin-differentiated social relationships and occasionally form coalitions against males. We established intersexual hierarchies across consecutive 6-month time blocks, representing either mating or birth seasons. Although females appeared to outrank 11% of males, they elicited male submission in only 2% of agonistic interactions against males. This discrepancy is likely due to the temporary residency of most males in the exceptionally large mandrill groups, the sexually coercive male mating strategies and the scarce number of agonistic interactions within most dyads, that may limit hierarchical inferences. In a second step, we found that the intersexual hierarchy mixes the intrasexual ones respecting their respective order. Females outranked mostly young and old males during the mating (vs. birth) season and social integration was positively correlated to dominance status in both sexes. In a third step, we found that females win more conflicts against young or old males which are closer to them in the intersexual hierarchy. These results extend our understanding of female-male dominance relationships by indicating that female mandrills occasionally outrank males who are considerably larger than them, and that a combination of demographic and social factors can influence the intersexual hierarchy.

Conflict over grooming topography between mandrill groomers and groomees

Grooming directed to different body areas is likely to imply different costs and benefits for groomers and groomees. In this study, we investigated social influences on grooming topography in captive female mandrills (Mandrillus sphinx). Subordinate groomers preferred to direct grooming to "safe" areas (the back and rump) compared to dominant groomers, while subordinate groomees did not solicit preferentially grooming to safe areas. Groomers tended to initiate grooming episodes from safe areas, while groomees solicited the switch to unsafe areas. Our results highlight a previously unrecognized source of conflict between the partners of grooming, one of the most common cooperative interactions in animals.

Odontochronologies in male and female mandrills (Mandrillus sphinx) and the development of dental sexual dimorphism.

We examine how dental sexual dimorphism develops in mandrills, an extremely sexually dimorphic primate. We aimed to (a) establish the chronology of dental development (odontochronology) in male and female mandrills, (b) understand interindividual and intersex variation in odontochronologies, and (c) determine how dental sexual dimorphism is achieved. We prepared histological ground sections from the permanent teeth of four female and four male mandrills from the semi-free ranging colony at the Centre International de Recherches Médicales, Franceville, Gabon. We used the microscopic growth increments in the sections to create odontochronologies. We compared ages at crown initiation, crown formation times (CFT) and crown extension rates (CER) between individuals and sexes to assess interindividual and intersex variation. All mandrill teeth are sexually dimorphic in size. Dental sexual dimorphism in mandrills is achieved via sex differences in the duration of growth (bimaturism) and in growth rates. We also found interindividual and intersex variation in the ages at initiation and completion of crown formation. Our results show that the rate of ameloblast differentiation varies between individuals and that selection for both the age at tooth initiation and CER has occurred independently in males and females to ensure that the teeth develop at appropriate times relative to the growth of the sexually dimorphic jaws. They also show that canine dimorphism is achieved through differences in both CER and CFT, unlike extant great apes or Cantius. Given at least three mechanisms for achieving canine dimorphism, we need more information to trace the evolution of this trait in primates.

The multidimensionality of female mandrill sociality-A dynamic multiplex network approach.

The structure and dynamics of primate social groups are shaped by the social relationships of its members. These relationships are based on different types of interactions and vary in relation to the identity of the interactants and over time. Social network analysis tools represent a powerful and comprehensive method to characterise social interactions and recent methodological advances now allow the study of the multidimensionality of sociality via multilayer networks that incorporate multiple types of interactions. Here, we use a multidimensional network approach to investigate the multidimensionality of sociality of females in a captive group of mandrills. We constructed two multiplex networks based on agonistic, proximity and grooming interactions of 6–7 mature females to analyse the multidimensionality of relationships within two independent observation periods; and three multiplex networks (one for each interaction type) to examine how relationships changed between periods. Within each period, different individuals were the most central in each layer and at the multiplex level, and different layers (i.e., interaction types) contributed non-redundant information to the multilayer structure. Across periods, relationships based on the same interaction type also contained non-redundant information. These results indicate that female mandrills engage in multidimensional and dynamic relationships, suggesting that in order to represent the full complexity of relationships, networks need to be constructed from more than a single type of interaction and across time. Our results provide evidence for the potential value of the multilayer network approach to characterise the multidimensionality of primate sociality.

Ecological, parasitological and individual determinants of plasma neopterin levels in a natural mandrill population.

Investigating how individuals adjust their investment into distinct components of the immune system under natural conditions necessitates to develop immune phenotyping tools that reflect the activation of specific immune components that can be measured directly in the field. Here, we examined individual variation of plasma neopterin, a biomarker of Th1 immunity in wild mandrills (Mandrillus sphinx), who are naturally exposed to a suite of parasites, including simian retroviruses and malaria agents. We analyzed a total of 201 plasma samples from 99 individuals and examined the effect of sex, age, social rank, reproductive state and disease status on neopterin levels. We found higher neopterin concentrations in males than females, but were unable to disentangle this effect from possible confounding effects of retroviral infections, which affect nearly all adult males, but hardly any females. We further detected a non-linear age effect with heightened neopterin levels in early and late life. In addition, adult males that harbored very high parasitaemia for Plasmodium gonderi also showed high neopterin levels. There was no effect of social rank in either male or female mandrills, and no effect of female reproductive state. Taken together, these results indicate that plasma neopterin may prove useful to investigate individual variation in investment into specific immune components, as well as to monitor the dynamics of immune responses to naturally occurring diseases that elicit a Th1 immune response.

A longitudinal molecular study of the ecology of malaria infections in free-ranging mandrills.

Unravelling the determinants of host variation in susceptibility and exposure to parasite infections, infection dynamics and the consequences of parasitism on host health is of paramount interest to understand the evolution of complex host-parasite interactions. In this study, we evaluated the determinants, temporal changes and physiological correlates of Plasmodium infections in a large natural population of mandrills (Mandrillus sphinx). Over six consecutive years, we obtained detailed parasitological and physiological data from 100 male and female mandrills of all ages. The probability of infection by Plasmodium gonderi and P. mandrilli was elevated (ca. 40%) but most infections were chronical and dynamic, with several cases of parasite switching and clearance. Positive co-infections also occurred between both parasites. Individual age and sex influenced the probability of infections with some differences between parasites: while P. mandrilli appeared to infect its hosts rather randomly, P. gonderi particularly infected middle-aged mandrills. Males were also more susceptible to P. gonderi than females and were more likely to be infected by this parasite at the beginning of an infection by the simian immunodeficiency virus. P. gonderi, and to a lesser extent P. mandrilli, influenced mandrills’ physiology: skin temperatures and neutrophil/lymphocyte ratio were both impacted, generally depending on individual age and sex. These results highlight the ecological complexity of Plasmodium infections in nonhuman primates and the efforts that need to be done to decipher the epidemiology of such parasites.

The dynamics of grooming interactions: maintenance of partner choice and the consequences of demographic variation for female mandrills.

A large body of evidence suggests that female Old World monkeys maintain selective long-term grooming interactions with fitness benefits. The last two decades have produced evidence that the regulation of social interactions among primates can be, in part, explained by the Biological Markets theory, with grooming behaviour as the focus of these studies. Grooming facilitates bonding between individuals, constituting an essential part of the regulation of social relationships among female cercopithecids. In contrast to the well-studied baboons (Papio spp), knowledge about the nature of grooming interactions and their regulation is generally lacking for the large, terrestrial species of mandrills (Mandrillus sphinx). We used a combination of social network analysis tools and well-established methods for assessing partner diversity and reciprocity to characterise grooming networks, partner choice and patterns of trade (be groomed, give grooming) among females in a captive group of mandrills, both within and across two separate observation periods. Our results suggest that, even though the relatively stable conditions of captivity allowed the studied females to maintain selective grooming interactions across time, small scale demographic changes affected the grooming dynamics of the group in accordance with the expectations of the Biological Markets theory. In particular, the maturation and consequent integration of a high ranking female into the group’s grooming network from one period to the next resulted in a more pronounced effect of rank on the regulation of grooming interactions. In addition, the influence of the maturation of a dependent infant on the grooming interactions of his mother were evident between periods. Our results also demonstrate that grooming networks are dynamic and that high ranking individuals are not necessarily the most central in grooming networks. Finally, we discuss the potential of social network analysis to identify cases of social exclusion and its consequences for captive management.

Competition for grooming partners and interference in affiliation among female mandrills

AbstractGrooming is the most common primate affiliative behaviour, and primates compete for accessing grooming partners. We studied a captive group of mandrills (Mandrillus sphinx) to evaluate the role of different types of competitive interactions in shaping the distribution of grooming among females. Mandrill females preferentially groomed high‐ranking individuals, but low‐ranking females were less able to do so. Interference in others’ grooming and a (consequent) reluctance of low‐ranking females to access dominant group mates occurred frequently and contributed to the observed pattern of grooming distribution, while takeovers of grooming partners was relatively rare. Interference in others’ affiliation was possibly used to prevent the formation of revolutionary alliances. Difficulties in accessing individuals already engaged in grooming exerted a strong but rank‐independent effect on grooming interactions. These results highlight the role of competition in determining access to preferred social partners.

Sternal Gland Scent-Marking Signals Sex, Age, Rank, and Group Identity in Captive Mandrills.

Mandrills are one of the few Old World primates to show scent-marking. We combined ethological and chemical approaches to improve our understanding of this behavior in 3 zoo-managed groups. We observed the olfactory behavior performed by adults and adolescents (N = 39) for 775h. We investigated the volatile components of sternal scent-marks using gas chromatography-mass spectrometry and compared volatile profiles with traits of the signaler. Males marked more than females and within each sex the frequency of scent-marking was related to age and dominance status, but alpha males scent-marked most frequently and particularly in specific areas at the enclosure boundaries. We identified a total of 77 volatile components of sternal gland secretion, including compounds functioning as male sex pheromones in other mammals, in scent-marks spontaneously released on filter paper by 27 male and 18 female mandrills. We confirmed our previous findings that chemical profiles contain information including sex, male age and rank, and we also found that odor may encode information about group membership in mandrills. Our results support the hypotheses that scent-marking signals the status of the dominant male as well as playing territorial functions but also suggest that it is part of sociosexual communication.

Androgens in a female primate: Relationships with reproductive status, age, dominance rank, fetal sex and secondary sexual color

A comprehensive understanding of the role of androgens in reproduction, behavior and morphology requires the examination of female, as well as male, hormone profiles. However, we know far less about the biological significance of androgens in females than in males. We investigated the relationships between fecal androgen (immunoreactive testosterone) levels and reproductive status, age, dominance rank, fetal sex and a secondary sexual trait (facial color) in semi-free-ranging female mandrills (Mandrillus sphinx), using samples collected from 19 reproductively mature females over 13months. Fecal androgens varied with reproductive status, being highest during gestation. Fecal androgens began to increase at 3months of gestation, and peaked at 5months. This pattern is more similar to that found in a platyrrhine than in other cercopithecine species, suggesting that such patterns are not necessarily phylogenetically constrained. Fecal androgens did not vary systematically with rank, in contrast to the relationship we have reported for male mandrills, and in line with sex differences in how rank is acquired and maintained. Offspring sex was unrelated to fecal androgens, either prior to conception or during gestation, contrasting with studies of other primate species. Mean facial color was positively related to mean fecal androgens across females, reflecting the same relationship in male mandrills. However, the relationship between color and androgens was negative within females. Future studies of the relationship between female androgens and social behavior, reproduction and secondary sexual traits will help to elucidate the factors underlying the similarities and differences found between the sexes and among studies.

Facial coloration tracks changes in women's estradiol

Red facial coloration is an important social cue in many primate species, including humans. In such species, the vasodilatory effects of estradiol may cause red facial coloration to change systematically during females' ovarian cycle. Although increased red facial coloration during estrus has been observed in female mandrills (Mandrillus sphinx) and rhesus macaques (Macaca mulatta), evidence linking primate facial color changes directly to changes in measured estradiol is lacking. Addressing this issue, we used a longitudinal design to demonstrate that red facial coloration tracks within-subject changes in women's estradiol, but not within-subject changes in women's progesterone or estradiol-to-progesterone ratio. Moreover, the relationship between estradiol and facial redness was observed in two independent samples of women (N = 50 and N = 65). Our results suggest that changes in facial coloration may provide cues of women's fertility and present the first evidence for a direct link between estradiol and female facial redness in a primate species.

Minimally invasive plate osteosythesis of fractures of the radius and ulna in a primate

A 25-year-old female mandrill (Mandrillus sphinx - a primate and part of the Old World monkey group) was presented with a mildly comminuted, diaphyseal, radial fracture associated with a transverse ulnar fracture. Minimally invasive plate osteosynthesis techniques were used to achieve fixation of both the radial and the ulnar fractures. First, closed fracture reduction was achieved with a distraction frame consisting of a motorized circular external skeletal fixator. Next, dual percutaneous radio-ulnar plating was performed using a 2.7 limited-contact dynamic compression plate on the cranial aspect of the radius and two stacked 2.0/2.7 veterinary cut-to-length plates on the lateral aspect of the ulna. Uncomplicated recovery was observed with a complete return to normal activity three months postoperatively. Fracture healing was documented at four weeks, clinical union at 14 weeks, and callus remodelling at 24 weeks postoperatively. This report demonstrates the feasibility of minimally invasive plate osteosynthesis in a primate and shows the adaptability of this technique across mammalian species.

Maternal Effects and the Endocrine Regulation of Mandrill Growth

Maternal effects can influence offspring growth and development, and thus fitness. However, the physiological factors mediating these effects in nonhuman primates are not well understood. We investigated the impact of maternal effects on variation in three important components of the endocrine regulation of growth in male and female mandrills (Mandrillus sphinx), from birth to 9 years of age. Using a mixed longitudinal set (N = 252) of plasma samples, we measured concentrations of insulin-like growth factor-I (IGF-I), growth hormone binding protein (GHBP), and free testosterone (free T). We evaluated the relationship of ontogenetic patterns of changes in hormone concentration to patterns of growth in body mass and body length, and determined that these endocrine factors play a significant role in growth of both young (infant and juvenile) and adolescent male mandrills, but only in growth of young female mandrills. We also use mixed models analysis to determine the relative contribution of the effects of maternal rank, parity, and age on variation in hormone and binding protein concentrations. Our results suggest that all of these maternal effects account for significant variation in hormone and binding protein concentrations in all male age groups. Of the maternal effects measured, maternal rank was the most frequently identified significant maternal effect on variation in hormone and binding protein concentrations. We suggest that these endocrine factors provide mechanisms that contribute to the maternal effects on offspring growth previously noted in this population.

Spontaneous Endometriosis in a Mandrill (Mandrillus sphinx)

A 25-year-old female mandrill (Mandrillus sphinx) died after exhibiting weakness and recumbency with serosanguineous ascites. Gross findings included haemoperitoneum and multifocal to diffuse serosal thickening with petechiae and ecchymoses throughout the peritoneum. The uterus was covered entirely with large blood clots and was adherent to the ovaries and pelvic wall. Microscopical and immunohistochemical examination revealed extra- and intra-uterine growth of ectopic endometrial tissue with marked fibrosis. The ectopic endometrial tissues predominantly consisted of stromal cells expressing CD10 and progesterone receptor and variably-sized glands lined by the epithelium with occasional slight expression of oestrogen receptor α. A diagnosis of endometriosis was made. This is the first report of naturally occurring endometriosis in a mandrill.

Chemical Composition of Scent-Gland Secretions in an Old World Monkey (Mandrillus sphinx): Influence of Sex, Male Status, and Individual Identity

Primates are traditionally considered to be microsmatic, with decreased reliance on olfactory senses in comparison to other sensory modalities such as vision. This is particularly the case for Old World monkeys and apes (catarrhines). However, various lines of evidence suggest that chemical communication may be important in these species, including the presence of a sternal scent-gland in the mandrill. We investigated the volatile components of mandrill odor using gas chromatography-mass spectrometry. We identified a total of 97 volatile components in 88 swabs of the sternal gland secretion and 95 samples of sternal gland hair saturated with scent-gland secretion collected from 27 males and 18 females. We compared odor profiles with features of the signaler using principle components and discriminant function analyses and found that volatile profiles convey both variable (age, dominance rank in males) and fixed (sex, possibly individual identity) information about the signaler. The combination of an odor profile that signals sex, age, and rank with increased motivation to scent-mark and increased production of secretion in high-ranking males leads to a potent signal of the presence of a dominant, adult male with high testosterone levels. This may be particularly relevant in the dense Central African rain forest which mandrills inhabit. By contrast, we were unable to differentiate between either female cycle stage or female rank based on odor profiles, which accords with behavioral studies suggesting that odor signals are not as important in female mandrills as they are in males. The similarity of our findings to those for other mammals and in primates that are more distantly related to humans suggests a broader role for odor in primate communication than is currently recognized.

Is Brightest Best? Testing the Hamilton-Zuk Hypothesis in Mandrills

Although many primates exhibit striking coloration, including brightly colored pelage and bare areas of skin, our understanding of the function and evolution of these traits pales in the face of knowledge about color in other taxa. However, recent years have seen an increase in the number of studies of individual variation in primate color and evidence is accumulating that these traits can act as important signals to conspecifics. Mandrills are arguably the most colorful of all primates. Here, we review what we have discovered about the signal function of coloration in male and female mandrills from our long-term studies of a semi-free-ranging colony in Franceville, Gabon and test the predictions of the Hamilton-Zuk hypothesis—that bright coloration is condition dependent, and that only individuals of superior quality will be able to express color fully—in this species. We compare measures of facial coloration in both sexes with parasite load (using fecal analysis over 1 annual cycle), immune status (hematological parameters), neutral genetic diversity (microsatellite heterozygosity), and major histocompatability (MHC) genotype to examine whether red coloration acts as an honest signal of individual quality in mandrills. We found that red coloration was unrelated to parasitism and hematological parameters. Red was also unrelated to genome-wide heterozygosity and MHC diversity, although specific MHC genotypes were significantly related to red. The healthy, provisioned nature of the colony and problems associated with observational, correlational studies restrict interpretation of our data, and it would be premature to draw conclusions as to whether color signals individual quality in mandrills. We conclude with some suggestions for future studies on the signal content of color in mandrills and other primates.

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.