Seed choice differs by sex in sooty mangabeys (Cercocebus atys).

The sooty mangabey (Cercocebus atys) practices year-round durophagy. A large part of the C. atys diet consists of the oily nut of Sacoglottis gabonensis, which is accessed by post-canine crushing of the hard, protective seed coat. During a typical foraging bout, some seeds are discarded after initial crushing attempts using isometric biting, but the reason mangabeys reject some seeds and break into others is unclear. Although C. atys is sexually dimorphic, little is known about whether differences between males and females affect the selectivity of mechanically protected foods. We studied C. atys feeding on S. gabonensis in the Taï National Park,  Côte d'Ivoire, in July and August 2016. Nuts discarded after an initial crushing attempt were collected and their hardness measured using a Shore D durometer. Measurements were taken in the region of the nut where monkeys attempted to crush it. Hardness values of nuts rejected by adult male (n = 79) and adult female (n = 104) C. atys were compared to those of a control assemblage of nuts collected randomly on the forest floor (n = 69). Nuts rejected by either sex do not differ statistically from the random sample; however, they do differ from each other, with females rejecting harder nuts. This suggests that males are more effective at broaching harder seed husks, and discard seeds based on other factors.

Sooty mangabeys scavenge on nuts cracked by chimpanzees and red river hogs-An investigation of inter-specific interactions around tropical nut trees.

Carrion scavenging is a well-studied phenomenon, but virtually nothing is known about scavenging on plant material, especially on remnants of cracked nuts. Just like meat, the insides of hard-shelled nuts are high in energetic value, and both foods are difficult to acquire. In the Taï forest, chimpanzees (Pan troglodytes) and red river hogs (Potamochoerus porcus) crack nuts by using tools or strong jaws, respectively. In this study, previously collected non-invasive camera trap data were used to investigate scavenging by sooty mangabeys (Cercocebus atys), two species of Guinea fowl (Agelestres meleagrides; Guttera verreauxi), and squirrels (Scrunidae spp.) on the nut remnants cracked by chimpanzees and red river hogs. We investigated how scavengers located nut remnants, by analyzing their visiting behavior in relation to known nut-cracking events. Furthermore, since mangabeys are infrequently preyed upon by chimpanzees, we investigated whether they perceive an increase in predation risk when approaching nut remnants. In total, 190 nut-cracking events were observed in four different areas of Taï National Park, Ivory Coast. We could confirm that mangabeys scavenged on the nuts cracked by chimpanzees and hogs and that this enabled them to access food source that would not be accessible otherwise. We furthermore found that mangabeys, but not the other species, were more likely to visit nut-cracking sites after nut-cracking activities than before, and discuss the potential strategies that the monkeys could have used to locate nut remnants. In addition, mangabeys showed elevated levels of vigilance at the chimpanzee nut-cracking sites compared with other foraging sites, suggesting that they perceived elevated danger at these sites. Scavenging on remnants of cracked nuts is a hitherto understudied type of foraging behavior that could be widespread in nature and increases the complexity of community ecology in tropical rainforests.

Mechanical adaptation of trabecular bone morphology in the mammalian mandible.

Alveolar bone, together with the underlying trabecular bone, fulfils an important role in providing structural support against masticatory forces. Diseases such as osteoporosis or periodontitis cause alveolar bone resorption which weakens this structural support and is a major cause of tooth loss. However, the functional relationship between alveolar bone remodelling within the molar region and masticatory forces is not well understood. This study investigated this relationship by comparing mammalian species with different diets and functional loading (Felis catus, Cercocebus atys, Homo sapiens, Sus scrofa, Oryctolagus cuniculus, Ovis aries). We performed histomorphometric analyses of trabecular bone morphology (bone volume fraction, trabecular thickness and trabecular spacing) and quantified the variation of bone and tooth root volumes along the tooth row. A principal component analysis and non-parametric MANOVA showed statistically significant differences in trabecular bone morphology between species with contrasting functional loading, but these differences were not seen in sub-adult specimens. Our results support a strong, but complex link between masticatory function and trabecular bone morphology. Further understanding of a potential functional relationship could aid the diagnosis and treatment of mandibular diseases causing alveolar bone resorption, and guide the design and evaluation of dental implants.

Jaw-Muscle Fiber Architecture and Leverage in the Hard-Object Feeding Sooty Mangabey are not Structured to Facilitate Relatively Large Bite Forces Compared to Other Papionins.

Numerous studies have sought to link craniofacial morphology with behavioral ecology in primates. Extant hard-object feeders have been of particular interest because of their potential to inform our understanding about the diets of early fossil hominins. Sooty mangabeys (Cercocebus atys) are hard-object feeders that frequently generate what have been described as audibly powerful bites at wide jaw gapes to process materially stiff and hard seeds. We address the hypothesis that sooty mangabeys have features of the masticatory apparatus that facilitate this feeding behavior by comparing fiber architecture and leverage of the masseter and temporalis muscles between sooty mangabeys and three papionin primates that do not specialize on hard objects. Contrary to predictions, sooty mangabeys do not have relatively larger muscle physiologic cross-sectional areas or weights compared to other papionins, nor do they consistently display improved leverage. In this regard, sooty mangabeys differ in their morphology from other hard-object feeders such as tufted capuchins. However, males of all four papionin species converge on a shared pattern of relatively longer anterior superficial masseter fibers compared with female conspecifics, suggesting that males are likely prioritizing muscle stretch to improve gape performance as part of a behavioral repertoire that includes agonistic social interactions and intense male-male competition. These findings strengthen support for the hypothesis that gape display behaviors can exert a strong selective influence throughout the musculoskeletal masticatory apparatus. Results also raise questions about the morphological suitability of extant cercopithecines as models for interpreting feeding behavior and diet in fossil hominins with limited jaw gape capacity. Anat Rec, 301:325-342, 2018. © 2018 Wiley Periodicals, Inc.

Spatial variation in mandibular bone elastic modulus and its effect on structural bending stiffness: A test case using the Taï Forest monkeys.

OBJECTIVES: We investigated how heterogeneity in material stiffness affects structural stiffness in the cercopithecid mandibular cortical bone. We assessed (1) whether this effect changes the interpretation of interspecific structural stiffness variation across four primate species, (2) whether the heterogeneity is random, and (3) whether heterogeneity mitigates bending stress in the jaw associated with food processing. MATERIALS AND METHODS: The sample consisted of Taï Forest, Cote d'Ivoire, monkeys: Cercocebus atys, Piliocolobus badius, Colobus polykomos, and Cercopithecus diana. Vickers indentation hardness samples estimated elastic moduli throughout the cortical bone area of each coronal section of postcanine corpus. For each section, we calculated maximum area moment of inertia, Imax (structural mechanical property), under three models of material heterogeneity, as well as spatial autocorrelation statistics (Moran's I, IMORAN ). RESULTS: When the model considered material stiffness variation and spatial patterning, Imax decreased and individual ranks based on structural stiffness changed. Rank changes were not significant across models. All specimens showed positive (nonrandom) spatial autocorrelation. Differences in IMORAN were not significant among species, and there were no discernable patterns of autocorrelation within species. Across species, significant local IMORAN was often attributed to proximity of low moduli in the alveolar process and high moduli in the basal process. DISCUSSION: While our sample did not demonstrate species differences in the degree of spatial autocorrelation of elastic moduli, there may be mechanical effects of heterogeneity (relative strength and rigidity) that do distinguish at the species or subfamilial level (i.e., colobines vs. cercopithecines). The potential connections of heterogeneity to diet and/or taxonomy remain to be discovered.

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

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

Correlations between social context and fecal glucocorticoid metabolite concentrations in free-ranging female gray-cheeked mangabeys (Lophocebus albigena) in Kibale National Park, Uganda.

An elevated concentration of glucocorticoids is an indicator of stress, and chronically high glucocorticoid levels are often associated with poor health and reduced fertility. We explored conditions that might be stressors in the lives of adult female gray-cheeked mangabeys (Lophocebus albigena) by measuring fecal glucocorticoid metabolites (fGCM) concentrations. During a six-month study we collected 109 fecal samples from 28 adult females from five groups in Kibale National Park, Uganda. We examined fecal fGCM levels of individual females relative to their own reproductive status (cycling or not cycling) and that of other females and to the presence of newcomer (immigrant) males. We found elevated fGCM concentrations in females when other females in their groups were at the peak of sexual swelling, and when immigrant males joined the group.

Hard-object feeding in sooty mangabeys (Cercocebus atys) and interpretation of early hominin feeding ecology.

Morphology of the dentofacial complex of early hominins has figured prominently in the inference of their dietary adaptations. Recent theoretical analysis of craniofacial morphology of Australopithecus africanus proposes that skull form in this taxon represents adaptation to feeding on large, hard objects. A modern analog for this specific dietary specialization is provided by the West African sooty mangabey, Cercocebus atys. This species habitually feeds on the large, exceptionally hard nuts of Sacoglottis gabonensis, stereotypically crushing the seed casings using their premolars and molars. This type of behavior has been inferred for A. africanus based on mathematical stress analysis and aspects of dental wear and morphology. While postcanine megadontia, premolar enlargement and thick molar enamel characterize both A. africanus and C. atys, these features are not universally associated with durophagy among living anthropoids. Occlusal microwear analysis reveals complex microwear textures in C. atys unlike those observed in A. africanus, but more closely resembling textures observed in Paranthropus robustus. Since sooty mangabeys process hard objects in a manner similar to that proposed for A. africanus, yet do so without the craniofacial buttressing characteristic of this hominin, it follows that derived features of the australopith skull are sufficient but not necessary for the consumption of large, hard objects. The adaptive significance of australopith craniofacial morphology may instead be related to the toughness, rather than the hardness, of ingested foods.

Sex and age differences in the diet and ingestive behaviors of sooty mangabeys (Cercocebus atys) in the Tai Forest, Ivory Coast.

Members of the Cercocebus-Mandrillus clade are united by several morphological features, including expanded premolars which are argued to be associated with a preponderance of hard objects in the diet. We test the association between premolar expansion and hard object feeding by examining how different dental regions are used during food processing. We examined the diet and oral processing activities of sooty mangabeys (Cercocebus atys) in the Ivory Coast's Tai forest from August 2008 to September 2009. In addition to compiling diet profiles, we recorded the frequency that individuals performed four activities: 1) incising, 2) canine puncturing/scraping, 3) postcanine crushing (i.e., isometric biting), and 4) routine mastication (chewing cycles). Sooty mangabeys have a relatively narrow diet that consists largely of nuts/seeds, fruits, and invertebrates. While there are age and sex differences in diet, the most frequently consumed foods are similar across age and sex classes. The most frequently consumed foods are seeds of Sacoglottis gabonensis which are the hardest items in the sooty mangabey diet. Patterns of ingestive behavior vary with food type, but adults and nonadults (excluding infants dependent on mothers) of both sexes process similar foods. Premolar expansion in Cercocebus atys is associated with powerful crushing of hard objects of specific size and durophagy is a constant feature of sooty mangabey feeding ecology throughout ontogeny.

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.