Assessment and preservation of liquid and frozen-thawed Black crested mangabey (Lophocebus aterrimus) spermatozoa obtained by transrectal ultrasonic-guided massage of the accessory sex glands and electroejaculation.

The Black Crested Mangabey (Lophocebus aterrimus) is an African monkey listed as Near Threatened by the IUCN and in captivity the population is limited to 34 males. The aim of this study was to evaluate two Black Crested Mangabey males, maintained in captivity in a zoological garden and suspected of infertility, with a complete examination of their genital tract using ultrasonography, followed by recovery of semen using transrectal ultrasonic massage of the accessory sexual glands (TUMASG) and electroejaculation. One male had small testicular and accessory sex gland sizes indicative of senile hypoplasia. The other male was suspected of infertility. Four semen samples were obtained. Fresh semen was initially evaluated, diluted in Refrigeration Medium Test Yolk buffer, cooled at 15 °C and cryopreserved. Endocrine profiles (testosterone, oestradiol, FSH, LH, cortisol), prostatic specific antigen and semen variables (volume, concentration, motility by CASA, viability and acrosome status using flow cytometry, morphology, morphometry utilising TEM) were evaluated in raw, cooled and cryopreserved samples. There was no detrimental effect of cooling or cryopreservation on sperm viability and acrosomal integrity. Similar percentages of viable and acrosome-intact spermatozoa were present in cooled (for 6 h) and frozen-thawed semen samples (75.1% compared with 69.0%, P > 0.05), while progressive motility was greater in cooled, compared with frozen-thawed samples (81.5% compared with 67.3%). This study was the first in which there was evaluation of sperm variables in this species and, although this study is limited by the number of animals it provides background information for further studies using assisted reproductive technologies.

Genetic assessment of an isolated endemic Samango monkey (Cercopithecus albogularis labiatus) population in the Amathole Mountains, Eastern Cape Province, South Africa.

The endemic Samango monkey subspecies (Cercopithecus albogularis labiatus) inhabits small discontinuous Afromontane forest patches in the Eastern Cape, KwaZulu-Natal midlands and southern Mpumalanga Provinces in South Africa. The subspecies is affected by restricted migration between forest patches which may impact on gene flow resulting in inbreeding and possible localized extinction. Current consensus, based on habitat quality, is that C. a. labiatus can be considered as endangered as the small forest patches they inhabit may not be large enough to sustain them. The aim of this study was to conduct a molecular genetic investigation to determine if the observed isolation has affected the genetic variability of the subspecies. A total of 65 Samango monkeys (including juveniles, subadults and adults) were sampled from two localities within the Hogsback area in the Amathole Mountains. Nuclear and mitochondrial DNA variation was assessed using 17 microsatellite markers and by sequencing the hypervariable 1 region (HVR1). Microsatellite data generated was used to determine population structure, genetic diversity and the extent of inbreeding. Sequences of the HVR1 were used to infer individual origins, haplotype sharing and haplotype diversity. No negative genetic factors associated with isolation such as inbreeding were detected in the two groups and gene flow between groups can be regarded as fairly high primarily as a result of male migration. This was in contrast to the low nuclear genetic diversity observed (H o = 0.45). A further reduction in heterozygosity may lead to inbreeding and reduced offspring fitness. Translocations and establishment of habitat corridors between forest patches are some of the recommendations that have emerged from this study which will increase long-term population viability of the subspecies.

Polyspecific associations of Cercopithecus campbelli and C. petaurista with C. diana: what are the costs and benefits?

Polyspecific associations (PSA) are common in many African primate communities, including the diurnal primates at Taï Forest, Côte d'Ivoire. In this paper I use data on the PSA of two forest guenons, Campbell's (Cercopithecus campbelli) and lesser spot-nosed monkeys (C. petaurista), with Diana monkeys (C. diana) and other primates to clarify interspecific relationships during 17 months including a 3-month low-fruit period. I analyzed association in relation to fruit availability and measured forest strata use for C. campbelli and C. petaurista when alone and in associations with and without C. diana. I also measured predator risk and reactions to potential predators. C. campbelli and C. petaurista had high association rates with C. diana monkeys, and fruit availability did not influence association rates. C. campbelli and C. petaurista used higher strata when in association with C. diana than when alone, but they used even higher strata when associated with other primates without C. diana. This suggested that C. diana competitively exclude C. campbelli and C. petaurista from higher strata. There were relatively large numbers of potential predators, and C. diana were usually the first callers to threatening stimuli, suggesting that antipredator benefits of association with C. diana outweighed the competitive costs. C. campbelli spent more time in association with C. diana than C. petaurista did and appeared to be more reliant on C. diana for antipredator benefits. C. petaurista were less reliant on C. diana because of a cryptic strategy and may have associated less in some months because of high chimpanzee (Pan troglodytes) presence.

The dangers of multi-male groupings: trauma and healing in cercopithecoid monkeys from Cameroon.

This study examines the potential linkage between social organization and trauma in a sample of cercopithecids from Cameroon. Skeletal trauma is described in a museum collection of eight sympatric monkey species. Macroscopic analysis was carried out on a total of 139 complete skeletons of mangabeys, colobines and guenons. Species in multi-male groups were found to have higher fracture frequencies than those in uni-male groups. These higher frequencies may be related to intra-specific male-male aggression; however, similarities in fracture patterning between males and females in multi-male groups suggest that other factors may be involved. Although fracture etiology may not be identified with certainty, this study suggests that predation may indirectly be a cause of traumatic injuries in those species of cercopithecid monkeys displaying multi-male social organizations. The data presented also highlight the utility of museum collections as an additional resource in analyses of primate behavior, demonstrating that behavioral information does not die when the animal does.

Female social relationships in a captive group of Campbell's monkeys (Cercopithecus campbelli campbelli).

A study group of Campbell's monkeys (Cercopithecus c. campbelli) provided data on affiliative and agonistic relationships between females. Over a period of two years (involving 111 hr), we conducted observations of a captive group which had a composition similar to wild groups. We were able to identify a monitor-adjust social system with frequent affiliative interactions, directed gazing and avoidances rather than aggressive acts. We described long-term differentiated affiliative bonds: adult females interacting more often with some group mates than others, especially if they were relatives. Interactions between matrilines concerned essentially play and young adult females. We found a significant linear hierarchy of dominance with rare reversals and a stable intermatriline dominance. In contrast to other single-male groups, our adult male was socially integrated into the group although this may have been because of the housing conditions. Comparisons with the social organization of other captive and wild guenon groups are discussed.

Comparative postcranial body shape and locomotion in Chlorocebus aethiops and Cercopithecus mitis.

Body weight and length, chest girth, and seven postcranial limb segment lengths are compared between two guenon species, Chlorocebus (Cercopithecus) aethiops (vervets) and Cercopithecus mitis (blue monkeys), exhibiting different habitual locomotor preferences. The subjects, all adults, were wild caught for a non-related research project (Turner et al. [1986] Genetic and morphological studies on two species of Kenyan monkeys, C. aethiops and C. mitis. In: Else JG, Lee PC, editors. Primate evolution, proceedings of the Xth International Congress of Primatology, Cambridge. London). The morphological results are interpreted within the context of previously published observations of primate locomotion and social organization. The sample is unique in that the body weight of each individual is known, allowing the effects of body-size scaling to be assessed in interspecific and intersexual comparisons. C. mitis has a significantly (P < 0.05) greater body weight and trunk length than C. aethiops. A shorter trunk may function to reduce spinal flexibility for ground-running in the latter. Proximal limb segments (arm and thigh) are significantly greater in C. mitis, reflecting known adaptations to committed arboreal quadrupedal locomotion. By contrast, relative distal limb segments (forearm, crus, and foot) are significantly longer in C. aethiops, concordant with a locomotor repertoire that includes substantial terrestrial quadrupedalism, in addition to arboreal agility, and also the requisite transition between ground and canopy. Although normally associated with arboreal monkeys, greater relative tail length occurs in the more terrestrial vervets. However, because vervets exploit both arboreal and terrestrial habitats, a longer tail may compensate for diminished balance during arboreal quadrupedalism resulting from the greater "brachial" and "crural" indices that enhance their ground quadrupedalism. Most interspecific differences in body proportions are explicable by differences in locomotor modalities. Some results, however, contradict commonly held "tenets" that relate body size and morphology exclusively to locomotion. Generally associated with terrestriality, sexual dimorphism (male/female) is greater in the more arboreal blue monkeys. A more intense, seasonal mating competition may account for this incongruity.

Patterns of vocal sharing and social dynamics in a captive group of Campbell's monkeys (Cercopithecus campbelli campbelli).

Although vocal sharing is widespread at several phylogenetic levels, few descriptions concerned primates. The present study involved the dynamics of vocal structures and social organization in a captive group of Campbell's monkeys (Cercopithecus campbelli campbelli) at 3-year periods, using precise sound recording and comparison. The authors focused on combined harmonic 6 calls, often involved in vocal exchanges and associated with approaches. Each female produced 1 to 4 variants, shared, or not, between individuals. Changes appeared between years in the form of disappearance, appearance, or transformation of variants. There was a decrease in the global degree of sharing over the years. Greater changes were observed after social disturbance. Sharing would be more important in disturbed than stable groups to advertise bonds.

A simple rule for the costs of vigilance: empirical evidence from a social forager.

It is commonly assumed that anti-predator vigilance by foraging animals is costly because it interrupts food searching and handling time, leading to a reduction in feeding rate. When food handling does not require visual attention, however, a forager may handle food while simultaneously searching for the next food item or scanning for predators. We present a simple model of this process, showing that when the length of such compatible handling time Hc is long relative to search time S, specifically Hc/S > 1, it is possible to perform vigilance without a reduction in feeding rate. We test three predictions of this model regarding the relationships between feeding rate, vigilance and the Hc/S ratio, with data collected from a wild population of social foragers (samango monkeys, Cercopithecus mitis erythrarchus). These analyses consistently support our model, including our key prediction: as Hc/S increases, the negative relationship between feeding rate and the proportion of time spent scanning becomes progressively shallower. This pattern is more strongly driven by changes in median scan duration than scan frequency. Our study thus provides a simple rule that describes the extent to which vigilance can be expected to incur a feeding rate cost.

Phylogenetic, paleodemographic, and taphonomic implications of Victoriapithecus deciduous teeth from Maboko, Kenya.

More than 240 milk teeth of Victoriapithecus macinnesi, representing all elements of the deciduous dentition, are described. Their morphology is intermediate between that of hominoids and cercopithecids. Unlike colobine and cercopithecine milk teeth, Victoriapithecus dp3s, dp4s, and at least 7 (14%) dp4s lack transverse distal loph(id)s and are not bilophodont. Victoriapithecus also differs from cercopithecids in having less elongated deciduous premolars, a dp3 metacone set mesial to a very small hypocone, a dp4 crista obliqua, and a dp4 hypoconulid. The deciduous canines and incisors of Victoriapithecus are like those of other cercopithecids in having an uneven distribution of enamel around a compressed (rather than cylindrical) root, but differ from cercopithecids and resemble hominoids in being more elongated. Since Colobinae and Cercopithecinae share features of the deciduous dentition that are derived relative to Victoriapithecus and hominoids, extant Old World monkeys are interpreted as representing the sister-taxon of the middle Miocene cercopithecoids. Due to a dramatic increase in the number of deciduous teeth found at Maboko Island, juvenile individuals represent a much larger proportion of recently excavated Victoriapithecus collections than is true of pre-1987 assemblages which mainly derive from sediment first excavated during the 1930s and 1940s. Age distribution differences between pre- and post-1987 samples indicate that paleontological collection procedures were more important than taphonomic biases in determining the paleodemographic profile of the Maboko fossils. Since the Victoriapithecus assemblage from Maboko is strikingly similar to that of fossil Theropithecus oswaldi from Olorgesailie in terms of the large number of specimens and high representation of juvenile and infant individuals, the latter can no longer be viewed as unique among cercopithecoid fossil assemblages. Rather than being related to a specific cause of death, such as selective hunting of T. oswaldi by Homo (Shipman et al. [1981] Curr. Anthropol. 22:257-268), the large number of cercopithecoids at both sites is attributed to the fact that both assemblages represent excavated samples and that the preferred habitats of the extinct monkeys were probably at or near the site of deposition. The greater number of young adult male than female canines in the apparently attritional Maboko Bed 5 assemblage, indicate that the social organization of V. macinnesi may have been similar to that of modern macaques, with males migrating out of their natal group and suffering higher death rates than females at puberty.

Some aspects of the monkey neurovirulence test used for the assessment of oral poliovirus vaccines.

Twelve years of experience in three control laboratories with 8,000 macaca monkeys for the testing of 204 monovalent lots of the three types of oral poliovirus vaccine (OPV), have shown that the new monkey neurovirulence test (MNVT) adopted by the World Health Organization (WHO) is a reproducible and sensitive assay likely to ensure the safety of this vaccine in humans. When the test vaccine and the appropriate homotypic reference vaccine were tested in a single group of monkeys, the concurrent use of the reference vaccine considerably increased the reproducibility of the test. The usefulness of the WHO MNVT was further demonstrated in our laboratory when the test was applied to types 1 and 3 vaccine strains that were passaged serially in the intestinal tract of infants. The test was suitable for detecting increased monkey neurovirulence in these human passage strains that did not reach the level of neurovirulence of the "wild" types 1 and 3 strains tested concurrently (except human passage no. 7 of the type 3 vaccine that multiplied for a cumulative 109 days in seven infants). The statistical analysis of the data showed that the old intrathalamic (IT) assay used for many years in our laboratory was considerably less sensitive than the intraspinal WHO MNVT; a test vaccine with a two-fold increase in monkey neurovirulence showed a 41% chance of failing in the IT test (using 30 monkeys per vaccine), while this chance increased to 99% in the WHO assay (using 12 monkeys for types 1 and 2 vaccines and 20 monkeys for type 3 vaccine). Indeed, three of seven type 3 lots tested in our laboratory with both assays failed in the WHO assay but all lots passed in the IT test. Since the introduction of the WHO MNVT in Canada and the United Kingdom, the number of vaccine-associated paralytic poliomyelitis cases in the population continued to remain at a low level.

Falsification of a single species hypothesis using the coefficient of variation: a simulation approach.

Dental variation remains an important criterion for assessing whether a morphologically homogeneous fossil primate sample includes more than one species. The Coefficient of Variation (CV) has commonly been used to compare variation in a fossil sample of unknown taxonomic composition with that of extant single-species samples, in order to determine whether more than one species might be present. However, statistical tests for differences between fossil and single species reference sample CVs often lack power, because fossil samples are usually small and confidence limits of the CV are consequently large. The present study presents a new methodology for using the CV to test the hypothesis that a sample represents only one species. Simulated sampling distributions of single-species and pooled-species CVs are generated based on variation observed in dental samples of extant Cercopithecus species. These simulated distributions are used to test a single-species hypothesis for 13 different combinations of two or three sympatric Cercopithecus species across four dental characteristics at different sample sizes. Two different ways to generate the reference value of the CV are used. Results show the proposed methodology has substantially greater power than previous methods for detecting multiple-species composition, while maintaining an acceptable Type I error rate. Results are also presented concerning the dependence of power on sample size and on the average difference between means in a pooled-species combination.

The genetic consequences of primate social organization: a review of macaques, baboons and vervet monkeys.

Primates, as long-lived, iteroparous, socially complex mammals, offer the opportunity to assess the effects of behavior and demography on genetic structure. Because it is difficult to obtain tissue samples from wild primate populations, research in this area has largely been confined to terrestrial and semi-terrestrial old world monkeys (e.g., rhesus and Japanese macaques, vervets and several subspecies of baboons). However, these species display a multi-male, multi-female social structure commonly found in many other primate and non-primate mammals. Electrophoretic analyses of blood proteins from individually recognized and/or marked wild Himalayan rhesus monkeys, themselves the subject of long-term behavioral and demographic research, have begun to reveal the genetic consequences of such phenomena as social group fission, male-limited dispersion, non-consanguineous mating patterns, and agonistically defined male dominance. Specifically, rhesus social groups, consisting primarily of clusters of maternal relatives, appear to be non-random samples of a population's genotypes and genes. The genetic effects of social group fission are highly dependent on each group's size, demographic structure, and average degree of relatedness. In all cases fission contributes to the degree of intergroup genetic differentiation. Male-limited dispersion appears both to retard genetic differentiation between social groups and to lead to mating patterns that result in an avoidance of consanguinity. Groups, therefore, appear to be genetically outbred. Comparing these results with studies of other free-ranging or wild cercopithecines allows several generalizations: (a) genetic variation seems to be evenly distributed throughout each local population of multi-male social groups; (b) social groups, however, because they contain clusters of relatives, are distinctive in their specific frequencies of genes; (c) the degree of genetic differentiation between a population's social groups, because of the effects of social group fission and non-deterministic forms of male dispersal, is somewhat greater than expected on the basis of migration rates alone; and (d) the asymmetrical pattern of dispersion with respect to sex effectively precludes inbreeding in any one social group or the population as a whole. These observations have important implications for understanding the unusually rapid rates of evolution among the primates.

Major dopamine innervation of the cortical motor areas in the cynomolgus monkey. A radioautographic study with comparative assessment of serotonergic afferents.

Dopamine (DA) and serotonin (5-HT) innervations were revealed by radioautography in primary motor, premotor and supplementary motor (SMA) cortex in Cynomolgus monkeys, using uptake of tritiated amines in vibratome sections under specific conditions that were previously established. DA and 5-HT axons were distributed throughout all cortical layers. A denser DA innervation was found in layers I, III and to a lesser extent layer V with a striking cluster-like arrangement in layer III, particularly in the SMA. 5-HT axons appeared less numerous; their lower density in comparison with DA axons was especially apparent in layer III, particularly in the premotor and motor areas. A DA-5-HT complementarity was thus suggested in this layer. These results suggest that in addition to the motor control exerted through the nigrostriatal pathway, the cortical DA projections could directly modulate the neuronal activity in motor areas. This could be of major importance in the pathophysiology of motor disorders such as Parkinson's disease.

An ancestral amplification of DNA in primates.

Newly evolved, tandemly arrayed, highly repeated DNAs from three primates were compared using Markov-chain and random-simulation approaches. Markov-chain calculations suggested that the repeated DNA sequences derived from the amplification of a progenitor sequence some 55 million years ago. Divergence of the products of this ancestral amplification could have created a library of related DNA sequences from which newly evolved repeated DNA was drawn - by recent amplifications of library members. The ancestral DNA amplification may have provided the genetic flexibility for creating the primate order; more recent amplifications in old-world primates probably led to the present subfamilies. The random-simulation approach verified the idea that repeated DNA evolves nonrandomly. A variable region was identified within the sequence.

Infanticide and social organization in the redtail monkey (Cercopithecus ascanius schmidti) in the Kibale Forest, Uganda.

The redtail monkeys of the Kibale Forest, W. Uganda, live in social groups of about 35 members with only one adult male. In one of the study groups the harem male was replaced by a new male from outside the group. This male-replacement was followed by the new male killing and eating two newborn infants in the group. Infants and young juveniles older than one month were not attacked. Following the infanticide the new male copulated with several adult females in the group. 8 months after this male joined the group, 5 other adult and subadult males associated with it. This multimale influx was accompanied by frequent and intense aggression among the males. Comparisons are made with the studies of langurs in India and Ceylon and it is suggested that infanticide following male-replacement in the harem affords reproductive advantages to the new male.