Craniomandibular morphology supporting the diphyletic origin of mangabeys and a new genus of the Cercocebus/Mandrillus clade, Procercocebus

Previous studies have noted skeletal and dental differences supporting the diphyletic origin of the mangabeys. Documented postcranial and dental characters are congruent with molecular data and thus support a close relationship between Cercocebus and Mandrillus (mandrills and drills) on the one hand and Lophocebus, Papio (baboons), and Theropithecus (geladas) on the other. Most of these characters, however, are postcranial and difficult to assess in the papionin fossil record because associated material is rare. In order to assess the African papionin fossil record and determine the evolutionary history of this group, cranial characters are critical. Here, a set of craniomandibular morphologies are documented that support the diphyletic origin of the mangabeys and more broadly support the molecular African papionin clades (i.e., Cercocebus/Mandrillus vs. Lophocebus/Papio/Theropithecus). These characters are then used to identify a series of fossil crania from Taung as representative of a new member of the Cercocebus/Mandrillus clade, Procercocebus antiquus. Procercocebus antiquus is closest in morphology to the extant taxon Cercocebus torquatus, and a probable ancestor-descendant relationship between Procercocebus and Cercocebus is suggested. Paleoecological reconstructions also suggest that a predator-prey relationship between African crowned eagles and the Procercocebus-Cercocebus lineage has existed for approximately the last two million years. Implications for Cercocebus biogeography and evolution are discussed.     

Molecular phylogeny of Old World monkeys (Cercopithecidae) as inferred from gamma-globin DNA sequences

DNA sequence data of the nuclear-encoded gamma1-gamma2-globin duplication region were used to examine the phylogenetic relationships of 16 cercopithecid (Old World monkey) species representing 12 extant genera. Morphology- and molecular-based hypotheses of Old World monkey branching patterns are generally congruent, except for generic relationships within the subtribe Papionina. The cercopithecids divide into colobines (leaf-eating monkeys) and cercopithecines (cheek-pouched monkeys). The colobines examined by the DNA data divide into an Asian clade (Nasalis, proboscis monkeys; Trachypithecus, langurs) and an African clade (Colobus, colobus monkeys). The cercopithecines divide into tribes Cercopithecini (Erythrocebus, patas monkey; Chlorocebus, green monkeys; Cercopithecus, guenons) and Papionini. Papionins divide into subtribes Macacina (Macaca, macaques) and Papionina (Papio, hamadryas baboons; Mandrillus, drills and mandrills; Theropithecus, gelada baboons; Lophocebus, arboreal mangabeys; Cercocebus, terrestrial mangabeys). In a morphologically based classification, Mandrillus is a subgenus of Papio, whereas Lophocebus is a subgenus of Cercocebus. In contrast, the molecular evidence treats Mandrillus as a subgenus of Cercocebus, and treats both Theropithecus and Lophocebus as subgenera of Papio. Local molecular clock divergence time estimates were used as a yardstick in a "rank equals age" system to propose a reduction in taxonomic rank for most clades within Cercopithecidae.     

Skeletal and dental morphology of African papionins: unmasking a cryptic clade

One of the more perplexing problems in primate systematics concerns the phyletic relationships of the large African monkeys--Mandrillus (including drills), Papio, Lophocebus and Cercocebus. For over twenty years, there has been molecular evidence that mangabeys are an unnatural group and that the terrestrial forms--Cercocebus--are the sister taxon of Mandrillus, while the arboreal forms--Lophocebus--are more closely allied with Papio. Nevertheless, most systematists have been reluctant to accept this scheme due to the lack of morphological evidence. In this paper, we undertake a detailed analysis of the scapula, humerus, radius, ulna, pelvis, femur and dentition of papionin primates. We identify a host of features shared by Cercocebus and Mandrillus to the exclusion of Lophocebus and Papio. The polarity of characters is established by examining an outgroup comprised of several species of Macaca. The features shared by Cercocebus and Mandrillus are functionally related to specific feeding and locomotor behaviors that include aggressive manual foraging, the processing of hard-object foods and the climbing of vertical trunks. We hypothesize that the ability to subsist on hard seeds and nuts gleaned from the forest floor is a key adaptation for the Cercocebus-Mandrillus clade.     

The banded karyotypes of Macaca fuscata compared with Cercocebus aterrimus

The karyotypes of Macaca fuscata and Cercocebus aterrimus are compared after G, C and AgNOR banding. Although it is often assumed that the 42-chromosome monkeys (species of the genera Macaca, Papio, and Cercocebus) are identical at the chromosomal level, a number of clear and consistent differences between the karyotypes of these two taxa are described. These differences include one pericentric inversion and differences in staining intensity, particularly in centromeric and pericentromeric areas. It is probable that high resolution chromosome techniques could reveal more differences between taxa in the 42-chromosome group than are now believed to exist. It is therefore probable that karyological data could provide insight into the phylogenetic relationships in this group of Old World monkeys.     

Brief communication: Enamel thickness and durophagy in mangabeys revisited

The documentation of enamel thickness variation across primates is important because enamel thickness has both taxonomic and functional relevance. The Old World monkeys commonly referred to as mangabeys have figured prominently in investigations of feeding ecology and enamel thickness. In this article, we report enamel thickness values for four mangabey taxa (Cercocebus atys, Cercocebus torquatus, Lophocebus aterrimus, and Lophocebus albigena), offer revised interpretation of the significance of thick enamel in papionin evolution, and place our new data in a broader comparative framework. Our data indicate that all mangabeys have thick enamel and that the values obtained for Cercocebus and Lophocebus equal or exceed those published for most extant non-human primates. In addition, new field data combined with a current reading of the dietary literature indicate that hard foods make up a portion of the diet of every mangabey species sampled to date. Clarification on the relationship between diet and enamel thickness among mangabeys is important not only because of recognition that mangabeys are not a natural group but also because of recent arguments that explain thick enamel as an evolved response to the seasonal consumption of hard foods.     

Molecular systematics of the old world monkey tribe papionini: analysis of the total available genetic sequences

The phylogenetic relationships among the genera of the tribe Papionini are inferred using a taxonomic congruence approach in which gene trees derived for eight unlinked genetic sequence datasets are compared. Population genetics theory predicts that species relationships will be revealed with greater probability when the topology of gene trees from many unlinked loci are found to be congruent. The theory underlying this approach is described. Monophyly of the mangabeys is not supported by any of the gene trees; instead, they are polyphyletic with Cercocebus found to be the sister taxon to Mandrillus in five gene trees (with no conflicting trees), and Lophocebus found to be closely related to Papio and/or Theropithecus in all trees. Theropithecus and Papio are not strongly supported as sister taxa (present in one or two trees only);Lophocebus and Papio are supported as sister taxa in the majority of trees. A close relationship between Mandrillus and Papio is not supported in any of the trees.The relationships among Papio, Lophocebus, and Theropithecus cannot be resolved by congruence, probably due to the short time interval estimated between their divergences. The mtDNA COII sequences are used to estimate divergence dates within the papionins. The internode between the divergences of these species is estimated to be between 290 ka and 370 ka. Lastly, the evolution of morphological features such as long faces, suborbital facial fossae, and terrestrial skeletal adaptations is discussed.     

Patterns of cranial shape variation in the Papionini (Primates: Cercopithecinae)

Traditional classifications of the Old World monkey tribe Papionini (Primates: Cercopithecinae) recognized the mangabey genera Cercocebus and Lophocebus as sister taxa. However, molecular studies have consistently found the mangabeys to be diphyletic, with Cercocebus and Mandrillus forming a clade to the exclusion of all other papionins. Recent studies have identified cranial and postcranial features which distinguish the Cercocebus-Mandrillus clade, however the detailed similarities in cranial shape between the mangabey genera are more difficult to reconcile with the molecular evidence. Given the large size differential between members of the papionin molecular clades, it has frequently been suggested that allometric effects account for homoplasy in papionin cranial form. A combination of geometric morphometric, bivariate, and multivariate methods was used to evaluate the hypothesis that allometric scaling contributes to craniofacial similarities between like-sized papionin taxa. Patterns of allometric and size-independent cranial shape variation were subsequently described and related to known papionin phylogenetic relationships and patterns of development.Results confirm that allometric scaling of craniofacial shape characterized by positive facial allometry and negative neurocranial allometry is present across adult papionins. Pairwise comparisons of regression lines among genera revealed considerable homogeneity of scaling within the Papionini, however statistically significant differences in regression lines also were noted. In particular, Cercocebus and Lophocebus exhibit a shared slope and significant vertical displacement of their allometric lines relative to other papionins. These findings give no support to narrowly construed hypotheses of uniquely shared patterns of allometric scaling, either between sister taxa or across all papionins. However, more general allometric trends do appear to account for a substantial proportion of papionin cranial shape variation, most notably in those features which have influenced traditional morphological phylogenies. Examination of size-uncorrelated shape variation gives no clear support to molecular phylogenies, but underscores the absence of morphometric similarities between the mangabey genera when size effects are controlled. Patterns of allometric and size-uncorrelated shape variation indicate conservatism of cranial form in non- Theropithecus papionins, and suggest that Papio represents the primitive morphometric pattern for the African papionins. Lophocebus exhibits a divergent morphometric pattern, clearly distinguishable from other papionins, most notably Cercocebus. These results clarify patterns of cranial shape variation among the extant Papionini and lay the groundwork for studies of related fossil taxa.     

Nuclear gene trees and the phylogenetic relationships of the mangabeys (Primates: Papionini)

Phylogenetic relationships of mangabeys within the Old World monkey tribe Papionini are inferred from analyses of nuclear DNA sequences from five unlinked loci. The following conclusions are strongly supported, based on congruence among trees derived for the five separate gene regions: (1) mangabeys are polyphyletic within the Papionini; (2) Cercocebus is the sister taxon to the genus Mandrillus; and (3) Lophocebus belongs to a clade with Papio and Theropithecus, with Papio as its most likely sister taxon. Morphologically based phylogenies positing mangabey monophyly were evaluated by mapping the sequences for each locus on these trees. The data seem to fit these trees poorly in both maximum-parsimony and likelihood analyses. Incongruence among nuclear gene trees occurred in the interrelationships among Lophocebus, Papio, and Theropithecus. Several factors that may account for this incongruence are discussed, including sampling error, random lineage sorting, and introgression.      

Behaviour of the Talapoin monkey (Miopithecus talapoin) studied in groups, in the laboratory

The behaviour of the Talapoin monkey has been studied both qualitatively and quantitatively by observing small captive groups kept in the laboratory. The behavioural repertoire is compared with that of other Old World Catarrhines. Talapoins show greater similarities to Cercopithecus monkeys than to Erythrocebus, Macaca, Papio or Cercocebus . However, there are differences in behaviour between talapoins and Cercopithecus monkeys, which lend additional support to the view that the former should be placed in the separate genus Miopithecus .     

Functional morphology of the mangabey mandibular corpus: relationship to dental specializations and feeding behavior

Recent molecular and morphological surveys suggest that mangabeys do not represent a monophyletic group. Specifically, Cercocebus is the sister taxon of Mandrillus, whereas Lophocebus forms an unresolved trichotomy with Papio and Theropithecus. The Cercocebus-Mandrillus clade is characterized by skeletal and dental adaptations related to acquisition and processing of hard-object foods that resist decomposition for months on the forest floor. Although species of both mangabey genera can be described as frugivorous seed predators with a strong reliance on hard-object foods, a growing body of evidence indicates that Cercocebus (terrestrial) and Lophocebus (arboreal) mangabeys differ in the hardness of the seeds they consume and the manner in which seeds are processed. The taxa are also distinguished on the basis of dental morphology. Given the purported differences in feeding behaviors of the two mangabey genera, we consider whether there are predictable biomechanical consequences of these behaviors that are reflected in mandibular corpus dimensions. In addition, we present metric data summarizing functional aspects of mangabey mandibular corpus morphology. Mangabey genera are generally not distinguished by differences in relative corpus size, either in postcanine or symphyseal regions. Distinct symphyseal scaling patterns characterize the Papio-Lophocebus clade and the Mandrillus-Cercocebus clade, while the postcanine corpus scales similarly between them. The hypothesis that preferential use of the incisors vs. premolars to initially process these foods results in distinct stress environments is weakly supported, given circumstantial evidence that the relative importance of bending vs. torsion may differ between Cercocebus and Lophocebus.     

Measurement of hemolytic complement and the third component of complement in nonhuman primates.

Complement, determined by hemolytic assay, and the third component of complement (C3), determined by radial immunodiffusion assay, were measured in nine nonhuman primate species. The species studied were the titi (Callicebus mollach). The sooty mangabey (Cercocebus atys), the thick-tailed galago or bushbaby (Galago crassicaudatus panganiensis), the crab-eating monkey (Macaca fascicularis), the rhesus monkey (Macaca mulatta), the bonnet monkey (Macaca radiata), the stumptailed macaque (Macaca speciosa), the yellow baboon (Papio cynocephalus), and the black-and-red tamarin (Saguinus nigricollis). Both sheep and bovine erythrocytes were used in the hemolytic complement assays. With the sheep erythrocyte system, sera from four species (yellow baboon, sooty mangabey, bonnet monkey, black-and-red tamarin) had similar titers with both antibody sensitized and non-sensitized erythrocytes. In contrast, the titers obtained using sensitized bovine erythrocytes was always higher than the values obtained using non-sensitized bovine erythrocytes. In all species, the titers for non-sensitized sheep erythrocytes was higher than the titer for non-sensitized bovine erythrocytes. When the species were compared for cross reactivity using the radial immunodiffusion assay for human C3, the rhesus monkey showed the strongest cross reaction; the thick-tailed galago, a prosimian, showed no detectable cross reactivity; and the other species examined showed intermediate degrees of reactivity.     

Ontogeny and phylogeny in papionin primates

This study investigates the developmental bases of size and shape variation in papionin primates (Macaca, Cercocebus, Mandrillus, Lophocebus, and Papio). The analysis tests hypotheses predicting that heterochronic changes in ontogeny, particularly in the degree of overall size growth, can account for cranial diversity and "allometric scaling" in this clade. Large developmental samples of extant papionin crania are examined to test heterochronic hypotheses using bivariate allometric methods. Analyses indicate that the crania of larger papionins (Mandrillus and Papio) are generally peramorphic, surpassing size and shape ranges of smaller, and probably less-derived, macaques and mangabeys. At least two heterochronic processes, including acceleration and hypermorphosis, can account for this pattern. Ontogenetic changes include decoupling of growth and development among cranial regions, along with simple shifts in size. Allometric scaling has complex developmental bases. Size change itself is not sufficient to explain all developmental differences among papionins, but these changes are extremely important in comparisons within cranial regions such as the face. Results imply that Papio exhibits strongly derived patterns of brain growth that impact postnatal patterns of size and shape transformation. Consideration of these results in the context of recent socioecological analyses suggests that derived patterns of cranial growth in Papio may be a response to selection during the early periods of ontogeny, resulting in a distinctive life history pattern.     

Chromosome identification in Macaca arctoides based on study of the differential staining pattern (G-discs). Comparison with Papio hamadryas G-discs]

Linear chromosome differentiation pattern of Macaca arctoides was studied using the Romanovsky-Gimsa stain (G-banding). The possibility of the identification of all chromosome pairs according to these data is demonstrated. The phenomenon of the irregular intercellular and chromosome differentiation is found out and a suggestion is made about its relation to a real mosaic functional activity of cell genomes. A great similarity in linear chromosome differentiation for 2 from 42 studied chromosome types of Macaca arctoides (genus Macaca) and Papio hamadryas (genus Papio) is shown. On the basis of these data it is supposed that in the divergency process of these species the chromosome microaberrations and molecular mutations played an important role, while large chromosome reconstructions were of no importance. The similar G-banding pattern of both metacentric chromosome arms in two species is found and this suggests an isochromosome mechanism of their occurance.     

Electrophoretic distances between the different species of mangabeys monkeys (author's transpl)]

The separation of the group of Mangabeys into two genera, Cerecocebus and Lophocebus, is justified by electrophoretic criteria. The same criteria permit assignment of the species aterrimus to an intermediary position within the second genus as well as the demonstration of the absence of differences between two species of Cercocebus.     

Common use of sleeping sites by two primate species in Tana River, Kenya

Choice of sleeping sites by two species of primates sharing two adjacent patches of gallery forest in Tana River, Kenya, was studied between August 1992 and February 1993. One group each of the Tana crested mangabey, Cercocebus galeritus galeritus Peters, and yellow baboon, Papio cynocephalus cynocephalus L., interchangeably shared nine sleeping sites distributed among four tree species, Acacia robusta Burch., Ficus sycomorus L., Abizzia gummifera (J. F. Gmel.) E. A. Sm. and Pachystela msolo (Engl.) Engl. The trees used by both species as sleeping sites were mainly tall trees with canopy level or emergent crowns. The trees had relatively larger crowns and lower percentage canopy cover compared to other trees at the site and were characterized by poor to moderate accessibility. Overlap in use of sleeping sites was never simultaneous and baboons occasionally supplanted mangabeys. Site choice by these two primates appeared to be influenced by predation risk, the feeding area used in the late afternoon, daily range and the availability of trees with the preferred structural characteristics. Sleeping sites appeared to be limited during and immediately after the wet season, when the frequency of supplantings increased. This observation is attributed to an increase in percentage canopy cover.     

Diet and habitat overlap in two sympatric primate species, the Tana crested mangabey Cercocebus galeritus and yellow baboon Papio cynocephalus

Diet and habitat overlap was studied in two sympatric primate species sharing two neighbouring patches of fragmented gallery forest in Tana River, Kenya. Systematic data on feeding and ranging behaviour was collected on one group each of the Tana crested mangabey Cercocebus galeritus and yellow baboon Papio cynocephalus between August 1992 and February 1993. When rainfall was low and fruit resources scarce, yellow baboons spent most of their foraging time in the open woodlands while mangabeys foraged within the forest. At this period, diet and habitat overlaps between the two species were low. As rainfall increased, followed by a gradual rise in fruit availability, yellow baboons shifted their foraging range and both species became confined to the forest habitat. Consequently, both diet and habitat overlaps increased, peaking at the end of the rainy season. Mangabeys showed a reduced within-group dispersal and also spent significantly less time foraging in a given forest patch when yellow baboons were also present within the same forest patch.
Increased habitat and diet overlaps during the wet season need not have resulted in increased interspecific competition for food because at this period, fruits were readily available in the forest.     

The lowest diploid number (2n = 16) yet found in any primate: Callicebus lugens (Humboldt, 1811)

Morphologic, molecular and karyologic analyses of Callicebus lugens (Humboldt, 1811) of known geographic origin supported the proposition that this is a valid species. Morphologic and morphometric analyses showed evident differences between C. lugens and two other related taxa of the same group (Callicebus purinus and Callicebus torquatus). Cytochrome b DNA analyses (maximum parsimony, neighbour joining and maximum likelihood) were congruent in showing a strong association between C. lugens and Callicebus sp. of the torquatus group in one branch and a sister branch further divided into two clades: one with species of the personatus group and another, with species of the moloch group. Karyotypic analysis showed that C. lugens has the lowest diploid chromosome number of the primate order (2n = 16). Comparisons with other congeneric species clearly supported the proposition that C. lugens is karyotypically similar to others of the torquatus group.     

Pregnancy,gestation and parturition in free-ranging tana river crested mangabeys (Cercocebus galeritus galeritus)

Mean gestation for seven free-ranging Tana River crested mangabeys (Cercocebus galeritus galeritus) is 180 days (SE = 4.49). All females showed postconception sexual swellings after the first 2 months of pregnancy, and two of the seven copulated with males at this time. One birth was observed; observations of a second infant began less than 1 hr after birth. Details of parturition are given, with responses of group members to the events. Adult and juvenile females showed more sustained interest in the new infants than adult or juvenile males.     

Incidence of chromosome aberrations in the bone marrow of monkeys and their progeny after exposure to aflatoxin B1

A mutagenic effect of aflatoxin B1 (AFB1) was studied in somatic cells of primates. It is shown that AFB1 elevates the chromosome aberration frequency in bone marrow cells of two monkey species: Macaca mulatta and Papio hamadryas. Genome mutations were found in these experimental primates simultaneously with chromosome aberrations. The AFB1-induced chromosome aberrations were revealed at least during two years of the study. The fact of the chromosome aberration frequency increase was established in Macaca babies born from females who received AFB1 in pregnancy.     

Interrelationships between Arixenia emu (Dermaptera) and molossid bats and their ectoparasites in Malaysia

Abstract. 1. Four species of Molossidae occur in Malaysia ( Cheiromeles torquatus and three Tadarida species) and from these, six species of potentially ectoparasitic insect have been recorded (two Etermaptera: Arixeniina; two Hemiptera: Cimicidae; two Siphonaptera: Ischnopsyllidae).
2. The two Arixeniina, Arixenia esau and Xeniaria jacobsoni are obligatorily associated with C. torquatus and only accidentally with Tadarida species with which C. torquatus often roosts. The nature of this association is presumed to be mutualistic and its origins are discussed.
3. A.esau can occur in great numbers in association with C.torquatus. It is primarily a roost dweller and is seldom found upon flying bats, although it is in this way that transference to new roosts must occur. It feeds mainly upon body exudates and skin debris from its hairless host. Aspects of its biology are discussed.
4. Arixenia species are usually found together with Xeniaria species but always greatly outnumber them. Differences between A.esau and X.jacobsoni are discussed.
5. The remaining four species of insect all feed upon blood and are truly parasitic, both species of bedbug and one flea being associated with C. torquatus and the other flea with Tadarida species. A.esau acts as a phoretic host for the flea host-specific to C. torquatus. Lagaropsylla turba. Otherwise no interactions were noted amongst the six insects.