Mandrills Research Articles

Mandrill (Mandrillus sphinx) Presence in Southeast Cameroon Confirmed By Camera Traps and Indigenous Knowledge

Mandrill (Mandrillus sphinx) Presence in Southeast Cameroon Confirmed By Camera Traps and Indigenous Knowledge

Granulomatous hepatitis caused by Calodium hepaticum in a captive mandrill (Mandrillus sphinx) in Brazil

The parasite Calodium hepaticum is a zoonotic, cosmopolitan nematode often associated with rodents. These nematodes have low host specificity and zoonotic potential, affecting the liver of their hosts. The objective of this work is to describe the first case, as far as the authors are aware, of C. hepaticum causing granulomatous hepatitis in captive Mandrillus sphinx. A necroscopic examination was performed and the organs were removed and evaluated; then, 1 cm³ fragments were collected and preserved in 10% buffered formalin. After fixation, the samples were submitted to histotechnical processing to make histological slides. At macroscopic examination, the liver showed heterogeneous red surface with light brown and whitish areas distributed throughout the parenchyma, with diverse punctiform structures measuring 1 to 3 mm in diameter. Histopathology revealed abundant multifocal granulomas with fibrosis and bioperculated barrel-shaped eggs, typical of C. hepaticum. Artificial tissue digestion of the liver was performed and the morphometric measurements of the parasite were as follows: 0.054 ± 0.002 mm in length, 0.031 ± 0.008 mm in width, wall thickness of 0.004 ± 0.0007 mm and opercula of 0.006 ± 0.001 mm. Parasitism was not the cause of death, but an incidental finding. However, further investigations are essential to choose control and prevention measures to prevent the infection of other animal groups and even humans. KEY WORDS: Nematoda; parasitism; primates; zoo medicine; wildlife pathology.

Circoviridae Survey in Captive Non-Human Primates, Italy.

Circoviruses (CVs) and cycloviruses (CyVs), members of the family Circoviridae, have been identified only occasionally in non-human primates (NHPs). In this study, we investigated the presence and genetic features of these viruses in 48 NHPs housed in the Bioparco-Rome Zoological Garden (Italy) and in the Anima Natura Wild Sanctuary Semproniano (Grosseto, Italy), testing fecal, saliva, and serum samples with a broadly reactive consensus nested PCR able of amplifying a partial region of the replicase (Rep) gene of members of the family Circoviridae. Viral DNA was detected in a total of 10 samples, including a saliva swab and 9 fecal samples collected, respectively from five Japanese macaques (Macaca fuscata) and four mandrills (Mandrillus sphinx), with an overall prevalence of 18.7% (9/48). On genome sequencing, five strains revealed the highest nucleotide identity (98.3-98.6%) to a CyV strain (RI196/ITA) detected in the intestinal content of a Maltese wall lizard (Podarcis filfolensis) in Italy. Although the origin of the Italian NHP strains, genetically distant from previously detected NHP CyVs, is uncertain, our results also highlight that the virome of captive animals is modulated by the different dietary and environmental sources of exposure.

Intersexual relationships in mandrills: dominance, sexual conflict and the influence of social integration

The conflict of evolutionary interests between the sexes is commonly imprinted in social dynamics and physical asymmetries between the sexes. In species that live in polygynandrous groups, male-biased sexual size dimorphism often allows males to socially dominate and sexually coerce females. Yet, smaller female size might allow females to escape from males and female philopatry might promote female-female social support allowing females to resist or retaliate against males. The study of such intersexual conflicts is highly relevant in mandrills (Mandrillus sphinx) as they form large polygynandrous groups and exhibit extreme male-biased sexual dimorphism in size and ornaments, higher social integration of females than males, and female coalitions against males. The set up of Mandrillus Project over a decade ago has offered a unique opportunity to study intersexual relationships of mandrills in their natural habitat. Here, I present a synthesis of some recent studies that used the long-term behavioural and life-history dataset of Mandrillus Project and documented patterns of sexual coercion and intersexual dominance in mandrills. These studies show that male mandrills are generally dominant over females and use sexual coercion to increase their mating success. However, female social bonds and social integration permit females to occasionally outrank certain males. Finally, and surprisingly, higher-ranking and more socially integrated females receive higher rates of male sexual coercion, highlighting the need for future research to shed light on the trade-offs between costs and benefits of mandrill sociality.

Stillbirth of a mandrill (Mandrillus sphinx) in the wild: perinatal behaviors and delivery sequences

Birth is a fundamental event in the life of animals, including our own species. More reports of wild non-human primate births and stillbirths are thus needed to better understand the evolutionary pressures shaping parturition behaviors in our lineage. In diurnal non-human primates, births generally occur at night, when individuals are resting. Consequently, they are difficult to observe in the wild and most of the current knowledge regarding perinatal behaviors comes from rare daytime births. Information about stillbirths is even rarer and their proximate causes are generally unknown. Here, we present detailed observations of a daytime birth of a stillborn wild mandrill (Mandrillus sphinx). During this event, which lasted an entire day, we recorded the behaviors of the parturient female ad libitum, using video recordings and photos. The 5-year-old female was primiparous and of low dominance rank. The length of her pregnancy was shorter than usual and the partum phase was extremely long compared to other birth reports in non-human primates. The female disappeared shortly after this event and was assumed to have died. We discuss the possible causes of this stillbirth including the infant’s presentation at birth and maternal inexperience.

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.

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.

Natural Non-Polio-Enteroviruses Detected in Captive Mandrills (Mandrillus sphinx) and Chimpanzees (Pan troglodytes troglodytes) Housed in a Primate Center in Franceville, Gabon

Natural Non-Polio-Enteroviruses Detected in Captive Mandrills (Mandrillus sphinx) and Chimpanzees (Pan troglodytes troglodytes) Housed in a Primate Center in Franceville, Gabon

Identification of potentially zoonotic parasites in captive orangutans and semi-captive mandrills: Phylogeny and morphological comparison.

Cysts and trophozoites of vestibuliferid ciliates and larvae of Strongyloides were found in fecal samples from captive orangutans Pongo pygmaeus and P. abelii from Czech and Slovak zoological gardens. As comparative material, ciliates from semi-captive mandrills Mandrillus sphinx from Gabon were included in the study. Phylogenetic analysis of the detected vestibuliferid ciliates using ITS1-5.8s-rRNA-ITS2 and partial 18S ribosomal deoxyribonucleic acid(rDNA) revealed that the ciliates from orangutans are conspecific with Balantioides coli lineage A, while the ciliates from mandrills clustered with Buxtonella-like ciliates from other primates. Morphological examination of the cysts and trophozoites using light microscopy did not reveal differences robust enough to identify the genera of the ciliates. Phylogenetic analysis of detected L1 larvae of Strongyloides using partial cox1 revealed Strongyloides stercoralis clustering within the cox1 lineage A infecting dogs, humans, and other primates. The sequences of 18S rDNA support these results. As both B. coli and S. stercoralis are zoonotic parasites and the conditions in captive and semi-captive settings may facilitate transmission to humans, prophylactic measures should reflect the findings.

Mother-to-daughter transmission of hygienic anti-parasite behaviour in mandrills.

Social animals are particularly exposed to infectious diseases. Pathogen-driven selection pressures have thus favoured the evolution of behavioural adaptations to decrease transmission risk such as the avoidance of contagious individuals. Yet, such strategies deprive individuals of valuable social interactions, generating a cost-benefit trade-off between pathogen avoidance and social opportunities. Recent studies revealed that hosts differ in these behavioural defences, but the determinants driving such inter-individual variation remain understudied. Using 6 years of behavioural and parasite data on a large natural population of mandrills (Mandrillus sphinx), we showed that, when parasite prevalence was high in the population, females avoided grooming their conspecifics' peri-anal region (PAR), where contagious gastro-intestinal parasites accumulate. Females varied, however, in their propensity to avoid this risky body region: across years, some females consistently avoided grooming it, while others did not. Interestingly, hygienic females (i.e. those avoiding the PAR) were less parasitized than non-hygienic females. Finally, age, dominance rank and grooming frequency did not influence a female's hygiene, but both mother-daughter and maternal half-sisters exhibited similar hygienic levels, whereas paternal half-sisters and non-kin dyads did not, suggesting a social transmission of this behaviour. Our study emphasizes that the social inheritance of hygiene may structure behavioural resistance to pathogens in host populations with potential consequences on the dynamics of infectious diseases.

Body mass estimates from postcranial skeletons and implication for positional behavior in Nacholapithecus kerioi: Evolutionary scenarios of modern apes.

This study reported the body mass (BM) estimates of the Middle Miocene fossil hominoid Nacholapithecus kerioi from Africa. The average BM estimates from all forelimb and hindlimb skeletal elements was 22.7 kg, which is slightly higher than the previously reported estimate of ~22 kg. This study revealed that Nacholapithecus has a unique body proportion with an enlarged forelimb relative to a smaller hindlimb, suggesting an antipronograde posture/locomotion, which may be related to the long clavicle, robust ribs, and some hominoid-like vertebral morphology. Because the BM of Nacholapithecus in this study was estimated to be below 30 kg, Nacholapithecus probably did not have relatively shorter and robust femora, which may result from other mechanical constraints, as seen in extant African hominoids. The BM estimate of Nacholapithecus suggests that full substantial modifications of the trunk and forelimb anatomy for risk avoidance and foraging efficiency, as seen in extant great apes, would not be expected in Nacholapithecus. Because larger monkeys are less arboreal (e.g., Mandrillus sphinx or Papio spp.), and the maximum BM among extant constant arboreal cercopithecoids is ~24 kg (male Nasalis larvatus), Nacholapithecus would be a constant arboreal primate. Although caution should be applied because of targeting only males in this study, arboreal quadrupedalism with upright posture and occasional antipronograde locomotion (e.g., climbing, chambering, descending, arm-swing, and sway) using the powerful grasping capacity of the hand and foot may be assumed for positional behavior of Nacholapithecus.

Successful acclimatization of mandrills (Mandrillus sphinx) translocated to Conkouati-Douli National Park, Republic of Congo, as measured by fecal glucocorticoid metabolites.

Translocation and reintroduction are common tools in conservation management and can be very successful. However, translocation can be stressful for the animals involved, and stress is implicated as a major cause of failure in release programs. Conservation managers should therefore seek to understand how the stages of translocation impact stress physiology in the animals involved. We quantified fecal glucocorticoid metabolites (fGCMs) as a noninvasive measure of response to potential stressors during a translocation of 15 mandrills (Mandrillus sphinx) into Conkouati-Douli National Park, Republic of Congo. The mandrills were initially housed in a sanctuary, transferred to a pre-release enclosure in the National Park and then released into the forest. We collected repeated fecal samples (n = 1101) from known individuals and quantified fGCMs using a previouslyvalidated enzyme immunoassay. Transfer from the sanctuary to the pre-release enclosure correlated with a significant 1.93-fold increase in fGCMs, suggesting that transfer was a stressor for the mandrills. fGCM values decreased over time in the pre-release enclosure, suggesting that the mandrills recovered from the transfer and acclimatized to the enclosure. Release to the forest was not linked to a significant increase in fGCMs over the final values in the enclosure. Following release, fGCMs continued to decrease, fell below sanctuary values after just over a month and were about half the sanctuary values after 1year. Overall, our results suggest that the translocation, although initially presenting a physiological challenge to the animals, was not detrimental to the well-being of the animals over the timescale of the study and, in fact,may have been beneficial. Our findings show the value of non-invasive physiology in monitoring, evaluating and designing wildlife translocations and, ultimately, contributing to their success.

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.

Effectiveness of buccal dental‐microwear texture in African Cercopithecoidea dietary discrimination

AbstractObjectivesThis study compares ISO (ISO/FDIS 25178) roughness parameters, calculated from three‐dimensional (3D) molar buccal microtexture surfaces, among African Cercopithecoidea primates with different diets.Materials and MethodsWe examined 98 lower second molars from seven African Cercopithecoidea species with diverse dietary regimes and habitat exploitation. Buccal dental surfaces were analyzed using a Sensofar Plu Neox laser scanning confocal microscope. Thirty‐eight, areal surface texture parameters were extracted (Mountain 7® software). Uni‐ and multivariate statistics were used to obtain diet‐related patterns of buccal‐microwear textures and feeding ecology to differentiate between species.ResultsBuccal‐dental 3D texture parameters discriminate between Cercopithecoidea diets. Analysis of variance (ANOVA) revealed significant variation in microwear texture between forest‐adapted Mandrillus sphinx, which showed coarse flat features, and grassland forager Theropithecus gelada, whose buccal surfaces were characterized by a high density of thin features. Buccal‐microwear textures of folivorous species (Colobus polykomos) were related to a lower density of thicker surface indentations in comparison to Papio anubis and Cercocebus atys which are adapted to the consumption of tough and hard foods. The limited interspecific variation in the buccal‐microwear textures of savanna dwellers (Chlorocebus pygerythrus and Chlorocebus aethiops) probably reflects similarities in their foraging diets.DiscussionSignificant variations between‐species demonstrate that 3D microwear ISO roughness parameters applied to buccal enamel surfaces can distinguish between the diets of Cercopithecoidea.

Range extension of the agile mangabey (Cercocebus agilis) and of the mandrill (Mandrillus sphinx) in eastern Gabon evidenced by camera traps

Range extension of the agile mangabey (<i>Cercocebus agilis</i>) and of the mandrill (<i>Mandrillus sphinx</i>) in eastern Gabon evidenced by camera traps

Estimation of the census (Nc) and effective (Ne) population size of a wild mandrill (Mandrillus sphinx) horde in the Lopé National Park, Gabon using a non-invasive genetic approach

Estimation of the census (Nc) and effective (Ne) population size of a wild mandrill (Mandrillus sphinx) horde in the Lopé National Park, Gabon using a non-invasive genetic approach

Sexual coercion in a natural mandrill population

Increasing evidence indicates that sexual coercion is widespread. While some coercive strategies are conspicuous, such as forced copulation or sexual harassment, less is known about the ecology and evolution of intimidation, where repeated male aggression promotes future rather than immediate mating success with targeted females. Although known in humans, intimidation was recently reported in chimpanzees (Pan troglodytes) and chacma baboons (Papio ursinus), where males are regularly violent against females. Here, we investigate the nature of male coercive strategies in wild mandrills (Mandrillus sphinx), a primate living in large polygynandrous groups where severe male aggression towards females is rare and females can form coalitions against males. Yet, we found support for all three predictions of the sexual coercion hypothesis, namely that male aggression (1) specifically targets sexually receptive females, (2) inflicts costs to these females, and (3) increases male mating success in the long-term. These results hold true when considering only non-physical threats, or only severe aggression. Finally, we show that high-ranking females are most targeted by males, probably because of their higher reproductive performances, while high-ranking males are most coercive. These results indicate that sexual intimidation is widespread in sexually dimorphic and group-living mammals, and that males and females vary in their propensities to use, and to be exposed to sexual coercion, respectively.

Prevalence and Molecular Identification of Entamoeba spp. in Non-human Primates in a Zoological Garden in Nanjing, China.

ObjectiveEntamoeba spp. are globally distributed zoonotic parasites that infect various hosts, among which non-human primates (NHPs) have been identified as one of the most common hosts of these parasites. Consequently, the infections of Entamoeba spp. in captive NHPs from Nanjing Hongshan Forest Zoo in China were investigated in order to assess their zoonotic potential.MethodsA total of 120 fresh fecal samples, including 19 species of NHPs, were collected from four breeding bases of the zoo from May to June 2019. The infections of six species of Entamoeba spp. were detected by PCR using the 16S or 18S rDNA-specific primers, and the positive samples were sequenced and analyzed.ResultsEntamoeba spp. were detected as positive in 59 NHPs fecal samples (49.17%), including five Entamoeba species: Entamoeba histolytica (7.50%), E. dispar (22.50%), E. coli (22.50%), E. chattoni (10.00%) and E. nuttalli (1.67%). Infection with one Entamoeba species was more common (35%) than co-infections (13.33%) or infections with three Entamoeba species (0.83%). There was a significantly higher prevalence rate of Entamoeba spp. in the species Pongo pygmaeus and Macaca mulatta than in Papio sp., Mandrillus sphinx, and Saimiri sciureus.ConclusionEntamoeba spp. are highly prevalent in the NHPs raised in Nanjing Hongshan Forest Zoo. Therefore, attention should be paid to the development of containment strategies of Entamoeba spp. in this zoological garden.

Fitness effects of seasonal birth timing in a long-lived social primate living in the equatorial forest

Reproductive seasonality is the norm in mammals from temperate regions but less common at lower latitudes, where a broad diversity of reproductive phenology strategies is observed. Our knowledge of the evolutionary determinants shaping this diversity remains fragmentary and may reflect high phenotypic plasticity in individual strategies. Here we investigated the ecological determinants and fitness consequences of variation in birth timing across the annual cycle in a social primate endemic to the Congo basin, the mandrill, Mandrillus sphinx , which breeds seasonally. We further examined traits that modulate this variation within and across individuals. We used 9 years of ecological, life history and behavioural data from a natural population to characterize patterns of environmental and reproductive seasonality. We then investigated the consequences of variation in birth timing for pre- and postnatal offspring survival and maternal interbirth intervals. Finally, we studied the influence of within- (reproductive history and age) and between-individual (social rank) traits on variation in birth timing. We found that mandrills’ daily foraging time varied seasonally, with greater fluctuations for subordinate than dominant females. Birth timing was plastic, as females gave birth year round without detectable consequences for postnatal offspring survival. Giving birth within the birth peak, however, decreased interbirth intervals and probability of miscarriage. Finally, reproductive history and social rank mediated within- and between-individual variation in birth timing, respectively. Specifically, females that experienced a previous reproductive failure gave birth early in the next birthing season and dominant females bred less seasonally than subordinates, which may reflect their more even access to resources across the year. Overall, the selective pressures shaping mandrill reproductive seasonality differed from a classical scenario of seasonal fluctuations in resources limiting offspring survival. A complex interplay between social and ecological factors may thus determine within- and between-individual variation in phenology strategies of tropical and gregarious mammals. • Mandrills breed seasonally in an equatorial environment. • Dominant females breed less seasonally than subordinate ones. • Interbirth intervals are minimized when giving birth inside the birth peak. • Offspring survival is not affected by birth seasonality. • Miscarriage probabilities increase when conceiving late in the mating season.

Advenella mandrilli sp. nov., a bacterium isolated from the faeces of Mandrillus sphinx.

A novel Gram-negative strain WQ 585T, isolated from the faeces of mandrills (Mandrillus sphinx) collected at Yunnan Wild Animal Park, Yunnan province, China, was subjected to a polyphasic taxonomic study. Phylogenetic analysis based on 16S rRNA gene sequences showed that the isolate belongs to the genus Advenella, sharing 98.5% and 98.2% sequence similarity with the type strain Advenella alkanexedens LAM0050T and Advenella faeciporci M-07T, respectively. The predominant ubiquinone was Q-8. The major cellular fatty acids (> 10%) were C16:0, C17:0cyclo and Summed Feature 2. The G + C content of the genomic DNA of strain WQ 585T was 49.0%. The whole genome average nucleotide identity (gANI) values of strain WQ 585T with strain A. alkanexedens LAM0050T and A. faeciporci M-07T were 86.7% and 86.7%, and the digital DNA-DNA hybridization values of strain WQ 585T with strain A. alkanexedens LAM0050T and A. faeciporci M-07T were 64.5% and 62.5%, respectively. Growth occurred at 10-45°C (optimally at 20-30°C), pH 6.0-9.0 (optimally at pH 7.0), and 0-5% (w/v) NaCl (optimally at 0.5-2.0%). On the basis of the taxonomic evidence, a novel species, Advenella mandrilli sp. nov., is proposed. The type strain is WQ 585T (= KCTC 82396T = CCTCC AA 2020028T).