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Volumetric comparisons in the cerebellar complex of anthropoids, with special reference to locomotor types.

Seven measurements in the cerebellar complex were completed on 45 individuals, including 26 species of anthropoids from Stephan's collection. These included 12 species of New World monkeys, 10 species of Old World monkeys, and Hylobates, Gorilla, Pan, and humans. The measurements were the volume of medial (fastigial) (CM), interpositus (globose and emboliform) (CI), and lateral (dentate) (CL) cerebellar nuclei, ventral pons (VPo), inferior olivary principal (OLIPr), and accessory (OLIAc) nuclei and vestibular nuclear complex (VES). The relative size of each nucleus was expressed in size indices based upon the allometric line obtained by the reduced major axis analysis. The indices of three cerebellar nuclei reflect the relative size of three longitudinal zones of the cerebellum. The cerebellar hemisphere-lateralis zone is represented by the CL indices, the vermis-medialis zone by the CM indices, and the pars intermedius-interpositus zone by the CI indices. The results show that the VPo and OLIPr indices are closely related to the CL indices. This lateral zone group of nuclei is the most progressively developed in humans, whereas the CM, CI, OLIAc, and VES are independent of the developmental trend manifest by the lateral zone group of nuclei. The indices are discussed in relation to the predominant locomotor pattern exhibited by a species. The size indices of arboreal quadrupeds show a development of all nuclei in the cerebellar complex. This is interpreted as indicating that arboreal monkeys live in complicated, discontinuous, three-dimensional space and need exceptional cerebellar capacity for each pattern of locomotion and positional behavior. Progressive development of the lateral zone group of nuclei only compared to other nuclei was recognizable in humans. This development is considered to be related not to bipedalism, but to versatile and coordinated finger movement, resulting after bipedalism was established. This cerebellar reorganization is also a prerequisite (Leiner et al. [1993] TINS 16: 444-447) for the evolution of human language. The differences between size indices of the nuclei of Macaca (= pronograde primate) and Ateles (= antipronograde one) are compared in relation to their vertical climbing kinesiological data.

Animals↗

Lack of hand preference in wild Hanuman langurs (Presbytis entellus).

Although there is a vast literature on laterality of hand-use in nonhuman primates, the Colobinae have been notably overlooked. Ten manual activities of differing complexity were studied in five male and five female adult Hanuman langurs (Presbytis entellus) from a well habituated, wild population at Ramnagar, in southern Nepal. The activities recorded were carry, eat, hit, hold, idle, manipulate, reach, retrieve, self-groom and social groom. This study aimed to examine handedness across tasks and across subjects in a natural population. The overall result was a lack of preference for subjects and patterns. Only in the eating activity did four individuals show significant hand preference, though they were not unidirectional. Eat seemed to be loosely associated with hold due to the requirements of the strata which the monkeys utilize. These results suggest that hand use is unlateralized in P. entellus. Those individuals exhibiting some hand preferences can be viewed as statistical exceptions or perhaps subject to experiential differences. The results are discussed in terms of their evolutionary significance and methodological implications.

Animals↗

Comparative locomotion and habitat use of six monkeys in the Tai Forest, Ivory Coast.

The relationships between locomotion, body size, and habitat use in six sympatric Old World monkeys are examined to test whether the associations found are consistent with those demonstrated in previous studies (Fleagle and Mittermeier [1980] Am. J. Phys. Anthropol. 52:301-314; Gebo and Chapman [1995] Am. J. Phys. Anthropol. 97:49-76). Colobus polykomos, C. badius, C. verus, Cercopithecus diana, C. campbelli, and Cercocebus atys were studied for 14 months in the Ivory Coast's Tai Forest. Analyses reveal that (1) larger monkeys tend to frequent those strata containing the greatest densities of large supports while smaller monkeys are more diverse in their canopy use; (2) high frequencies of leaping are not necessarily confined to the understory, and understory specialists are not necessarily frequent leapers; (3) body size does not consistently predict leaping or climbing frequencies; (4) in general, climbing is more frequent during foraging and leaping is more common during travel; (5) larger supports are used during travel while smaller supports are used during foraging; and (6) larger monkeys do not always use larger supports than do smaller monkeys. Some of the factors contributing to the manner that locomotion, body size, and habitat use are related in cercopithecid monkeys are discussed.

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Analysis of the short wavelength-sensitive ("blue") cone mosaic in the primate retina: comparison of New World and Old World monkeys.

The distribution of short wavelength-sensitive (SWS or "blue") cone photoreceptors was compared in primates with dichromatic ("red-green colour blind") and trichromatic colour vision. We compared a New World species, the marmoset (Callithrix jacchus), with an Old World species, the macaque monkey (Macaca nemestrina). The SWS cones were identified by their immunoreactivity to an antiserum against the human SWS cone opsin. A single retina from a male capuchin monkey (Cebus apella) also was studied. The SWS cones make up less than 10% of all cone photoreceptors throughout the retina of all animals studied. In marmoset, the peak spatial density of SWS cones is close to 10,000/mm2 at the foveola. In macaque, the peak spatial density of SWS cones, close to 6,000/mm2, is at the fovea, but SWS cones are absent within 50 microm of the centre of the foveola. In both species, the density of SWS cones is higher on the nasal retinal axis than at corresponding eccentricities on the other retinal axes. The SWS cones in macaque are arranged in a semiregular array, but they are distributed randomly in marmoset. There is no difference in the spatial density or local arrangement of SWS cones between dichromatic and trichromatic marmosets. The results suggest that the SWS cone photoreceptor system is subject to different developmental and evolutionary constraints than those that have led to the formation of the red-green photoreceptor systems in primate vision.

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Determinants of female dispersal in Thomas langurs.

Female dispersal occurs in a number of primate species. It may be related to: avoidance of inbreeding, reduction in food competition, reduction of predation risk, or avoidance of infanticide in combination with mate choice. Female dispersal was studied for a 5-year period in a wild population of Thomas langurs (Presbytis thomasi) that lived in one-male multi-female groups. Juvenile and adult individuals of both sexes were seen to disperse. Females appeared to transfer unhindered between groups, mostly from a larger group to a recently formed smaller one. They transferred without their infants and when not pregnant, and seemed to transfer preferentially during periods when extra-group males were harassing their group. During these inter-group encounters extra-group males seemed to try to commit infanticide. Thus, the timing of female transfer was probably closely linked to infanticide avoidance. Moreover, females seemed to transfer when the resident male of their group was no longer a good protector. The observations in the present study suggest that females transferred to reduce the risk of infanticide. Female dispersal may have another ultimate advantage as well, namely inbreeding avoidance. Due to the dispersal of both females and males the social organization of Thomas langurs was rather fluid. New groups were formed when females joined a male; male takeovers were not observed. Bisexual groups had only a limited life span, because all adult females of a bisexual group could emigrate. This pattern of unhindered female dispersal affects male reproductive strategies, and in particular it might lead to infanticidal behavior during inter-group encounters.

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The menstrual cycle of the spider monkey (Ateles geoffroyi).

The ovarian cycles of four adult female spider monkeys (Ateles geoffroyi) were followed daily throughout 30 days by means of vaginal swabs and blood samplings. Cytological analyses of the vaginal swabs and radioimmunoassay determination of the daily levels of estradiol-17 beta (E2) and progesterone (P4) wer done in order to classify the kind of ovarian cycle of this species. Our results show that Ateles geoffroyi females display menstrual cycles of about 24 days on average. By comparison with the well-known menstrual cycles of women, apes, and Old World monkeys, the four distinctive cytological phases (bleeding, follicular, periovulatory, and luteal) could be recognized; mid-cycle E2 peaks followed by mid-luteal increases of the same hormone were present in all four females. P4 levels were higher after the E2 peak, although both hormones were present throughout the cycles. Also, age-dependent features, hormone profiles, and changes in menstrual phases lengths were detected.

Analysis of Variance↗

Female dispersal, social organization, and infanticide in langurs: are they linked to human disturbance?

Female dispersal in gregarious animals can involve the desertion of a site, desertion of a social group, or both. Group desertion may be related to inbreeding avoidance. Group fidelity may result from cooperation among females in a group. Site fidelity will be more likely when food can be monopolized and when the population density is close to habitat saturation. The degree of habitat saturation was approximated with a measure of human disturbance. The influence of these various factors on the incidence of female dispersal was investigated for langur populations using data from the literature. The results suggest that female dispersal in langurs involved site desertion, not group desertion. The incidence of female dispersal may affect the social organization of langurs. I propose that when females do not disperse, male takeovers prevail, whereas in populations where female dispersal regularly occurs bisexual groups are disbanded or new groups are formed, a process I call female split-merger. Male takeover is thought to occur when site fidelity is high, female split-merger when site fidelity is low. These processes were indeed found to occur in these circumstances. The dispersal of females might prevent infanticide, whereas male takeover might promote it. Indeed, in studies with male takeover, more infants fell victim to infanticide than in studies with female split-merger. Therefore, female dispersal in langurs is an effective female counterstrategy to infanticide. The factor that had the most profound effect on female dispersal, social organization, and infanticide was habitat saturation. Habitat saturation was measured as the degree of human disturbance, and its influence on the behavior of langurs is probably of relatively recent date. This may lead to an evolutionary transient situation and may explain the discrepancy between current socioecological theories and the behavior of langurs in populations lacking female dispersal.

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Hormonal correlates of reproductive seasonality in wild female hanuman langurs (Presbytis entellus).

To date, it is not known whether the seasonal occurrence of sexual behavior and mating in free-ranging Hanuman langurs at Ramnagar, Nepal, is correlated with seasonal changes in female ovarian function, and, if so, which factor(s) triggers the onset of the reproductive period. Using noninvasive fecal hormone analysis in combination with behavioral observations, this study was carried out to: 1) investigate and characterize seasonal patterns of ovarian cyclicity and timing of conception in wild langur females living in a highly seasonal habitat; and 2) examine the relationship between seasonal patterns of ovarian cyclicity, behavioral estrus, and female physical condition. Behavioral data and fecal samples were collected during a total period of 14 months from nine females living in a multi-male group. Physical condition of the females was assessed monthly by visual inspection, using a seven-fold scale. Ovulatory cycles and timing of conceptions were identified by the measurement of immunoreactive pregnanediol glucuronide (iPdG) in extracted feces. Hormone profiles in individual females revealed a clearly seasonal distribution in the occurrence of ovulatory cycles, which were restricted to the period from July to October. The distribution of female estrus behavior showed a similar seasonal pattern, and in total 88.2% of all estrus periods observed in the focal females were accompanied by ovulation. Onset of ovarian cycles as well as mating activities were strongly correlated with the onset of the rainy season. Females conceived, on average, in their second ovulatory cycle (pregnancy length: 211.6 +/- 3.4 days), with timing of conception being confined to the months when animals showed an improved physical condition. Collectively the present data clearly suggest that in seasonally-breeding langurs at Ramnagar, ecological conditions (rainfall, food availability, and quality) influence the onset of ovulations and timing of conceptions.

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Nuclear integrations of mitochondrial DNA in primates: inference of associated mutational events.

To infer the possible mutational events taking place along the interorganellar transfer of genetic material from mitochondria to the nucleus, four integrations of mitochondrial DNA (mtDNA) in the human genome were characterized together with their flanking nuclear sequences. By determining their presence/absence status in different primate species, these integrations were inferred to have occurred on the lineages leading to catarrhines (Old World monkeys and hominoids), to hominoids and to humans, respectively. In case of a polymorphic state, with respect to its presence in a certain species, each preintegration sequence was either cloned in the same species or in a primate taxon that branched off before the transfer of the mtDNA to the nucleus took place. For the four mtDNA integrations presented here, random mobilization of the mtDNA and differing mechanisms for generating free ends in the nuclear target sequences can be inferred. Additionally, no common sequence features at the preintegration sites could be observed for these integrations. Moreover, the comparisons of the sites before and after integration suggest different ways of integration. Thus, mtDNA integrations represent unique molecular recombinations in the evolutionary history and can, according to their presence/absence status in different species, help to determine the branching order in phylogenetic trees.

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Thalassemia: recent insights into molecular mechanisms.

Recent advances in defining the molecular basis for the thalassemia syndromes are discussed. We now realize that the causes of the thalassemia phenotype are diverse and include gene deletions, nuclear RNA processing defects, nonsense mutations, fusion genes, termination codon mutants, and unstable globin chains.

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Comparative energetics of primate fetal growth.

Among the primates, Homo sapiens has evolved a life history which includes long gestation, relatively slow growth to reproductive maturity, and large body size. While the slow growth rate may be linked to the energetic demands of having a large brain, there are other important morphological and physiological linkages that may be adaptive, including the development of significant fat stores with which to buffer against episodic and periodic energetic stress. In this comparative analysis of the energetic burden of pregnancy among primates (including humans), the daily energy investment in the development of neonatal tissue is modeled. During pregnancy, larger primates, notably the Hominidae, invest a smaller proportion of their maternal daily nonmaintenance energy budget in fetal tissue with increasing energy budget, allowing diverse adaptations, including foraging strategies which include folivory and mixed patterns of food getting, and meat consumption. Humans have a similar proportion of maternal daily nonmaintenance energy budget invested in fetal tissue with increasing energy budget to other apes and have a diet which is of much higher quality than predicted for body size and metabolic needs. The combination of high diet quality and low proportion of maternal daily nonmaintenance energy budget invested in fetal tissue allows greater brain size relative to body weight at birth compared with all other primates, apart from chimpanzees, and higher birthweight and body fatness at birth for a given body size than other primate species.

Analysis of Variance↗

Possible audience effect in Thomas langurs (Primates; Presbytis thomasi): an experimental study on male loud calls in response to a tiger model.

Recent research indicates that animal vocalizations can refer to objects in the outside world, and that call production may be controlled by the sender depending on the type of audience involved. Our research on wild male Thomas langurs (Primates: Presbytis thomasi) shows that these males call as a response to a tiger model when they are in a group, but do not call when they are solitary. This is the first experimental study on wild primates to demonstrate that the presence or absence of an audience influences calling behavior. Our results indicate that males in mixed-sex groups give more loud calls than solitary males when exposed to a predator model. This suggests that giving loud calls in response to predators is not purely a reflex and may be controlled in some way by the sender.

Animal Communication↗

Effect of diet on dental development in four species of catarrhine primates.

In this study, dental development is described in two pairs of closely related catarrhine primate species that differ in their degree of folivory: 1) Hylobates lar and Symphalangus syndactylus, and 2) Papio hamadryas hamadryas and Semnopithecus entellus. Growth increments in histological thin sections are used to reconstruct the chronology of dental development to determine how dental development is accelerated in the more folivorous species of each pair. Although anterior tooth formation appears to be unrelated to diet, both S. syndactylus and S. entellus initiate the slowest-forming molar earlier than the related less-folivorous species, which supports the hypothesis that dental acceleration is related to food processing. S. syndactylus initiates M2 crown formation at an earlier age than H. lar, and S. entellus initiates and completes M3 at an earlier age than P. h. hamadryas. Similar stages of M3 eruption occur earlier in the more folivorous species; however, the sex of the individual may also play a role in creating such differences. Although the age at M3 emergence is close to that reported for the end of body mass growth in lar gibbons, hamadryas baboons, and Hanuman langurs, M3 emergence may not be coupled to body mass growth in siamangs.

Age Determination by Teeth↗

Status and distribution of golden langurs (Trachypithecus geei) in Assam, India.

The distribution of golden langurs (Trachypithecus geei) is limited to a small area of western Assam in northeast India and Bhutan between the rivers Manas in the east, Sankosh in the west, and Brahmaputra in the south. It is one of the most seriously endangered primate species of India. A comparative analysis based on satellite images taken in 1988 and 1998 showed a 50% loss of original golden langur habitat. Data on population dynamics collected using line transect and total count methods are presented here. An average group size of 8.2 (range 4.0-22.0) individuals was recorded. A total of 1,064 individuals were counted living in 130 groups. The sex ratio was 1.9-2.5 adult females for each adult male. A low percentage of juveniles and infants suggests that the population is unstable. Most of the groups had only one adult male. Small group sizes, isolated distribution, proportionately few infants and juveniles, and degrading habitat are all causes of concern. Demographic trends indicate a decline in the golden langur population.

Animals↗

Differential energy budget and monopolization potential of harem holders and bachelors in Hanuman langurs (Semnopithecus entellus): preliminary results.

The demographic structure in the Hanuman langur (Semnopithecus entellus) population of Jodhpur is extreme, in that some single males monopolize harems with, on average, 25 adult females. It has been proposed that extratroop males, which live in all-male bands, inhabit low-quality habitats and suffer from reduced food provisioning and longer daily travel distances. To compare the resulting energetic consequences for harem holders and bachelors, I estimated their gross energy intake and daily energetic expenditures. This analysis revealed no clear-cut differences between the two classes of males in time spent feeding on provisioned food, daily path length, gross energy intake, and energy expenditure. Due to the small sample size and other limitations of the study design, the hypothesis under investigation can not be evaluated conclusively. The preliminary results suggest, however, that energy budgets of harem holders and bachelors do not differ markedly. The importance of direct ecological pressures to males for our understanding of variation in group composition is highlighted.

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Changes of urinary steroid conjugates and gonadotropin excretion in the menstrual cycle and pregnancy in the Yunnan snub-nosed monkey (Rhinopithecus bieti).

The Yunnan snub-nosed monkey (Rhinopithecus bieti) is one of the most endangered species in the world, and it is endemic to China. According to our knowledge, there was no information on reproduction for this species. The present study was designed to understand the characteristics of reproductive hormone secretion during the menstrual cycle and pregnancy of this species by monitoring urinary estrone conjugate (E1C), pregnanediol-3-glucuronide (PdG), bioactive follicle-stimulating hormone (FSH), and luteinizing hormone (LH). The urine samples were collected each day from four adult females for eight menstrual cycles, and once in 3 days during pregnancy (three full-term pregnancies, one mid-term abortion). The steroid conjugate was tested by radioimmunoassays (RIAs), and bioactive FSH and LH levels were measured in vitro by the sensitive bioassays granulosa cell aromatize bioassay (GAB) and rat interstitial cell testosterone (RICT), respectively. The results showed that: 1) E1C presented a preovulatory peak (183.9 +/- 8.6 ng/mgCr) followed by a definite elevation of PdG; 2) PdG in the luteal phase (754.4 +/- 30.6 ng/mgCr) was three- to fivefold higher than during the corresponding follicular phase (198.3 +/- 11.4 ng/mgCr); 3) the peaks of bio-LH and bio-FSH were on the same day, while the E1C peak was 1 or 2 days before the peaks for these two hormones; 4) bio-FSH levels were higher in the follicular phase than in the luteal phase, and bio-LH levels elevated slightly in the luteal phase; 5) the mean cycle length was 23.6 +/- 3.5 days (n = 3) based upon successive urinary LH peaks; 6) based on the interval from the day of E1C peak to the day of parturition, the gestation was 203.7 +/- 2.5 days (n = 3); and 7) both E1C and PdG increased and remained high after pregnancy, with a sharp decrease in basal levels following parturition or mid-term abortion. The results suggested that the pattern of reproductive hormones for R. bieti is similar to that of other Old World monkeys, but the concentration of the hormones is different from that of other species. This species has a longer progestation period, which may be related to its classification status.

Animals↗

Ancestral loss of the maxillary sinus in Old World monkeys and independent acquisition in Macaca.

Cercopithecoid monkeys are unique among primates in that all species (except macaques) lack a maxillary sinus, an unusual condition among eutherian mammals. Although this uncommon distribution of cranial pneumatization was noted previously, the phylogenetic ramifications have not been investigated fully. Recently, character state optimization analysis of computed tomography (CT) data from extant Old World monkeys suggested that the loss of the sinus may have occurred at the origin of the group, unlike previous hypotheses positing only a reduction in size of the structure. To critically evaluate the "early loss" hypothesis, a recently recovered complete cranium of Victoriapithecus macinnesi from Maboko Island, Kenya, was examined by CT to determine the extent of its cranial pneumatization. This taxon is crucial for evaluating character state evolution in Old World monkeys, due to its phylogenetic position, preceding the cercopithecine/colobine split. CT analysis reveals only cancellous bone lateral of the nasal cavity, indicating that Victoriapithecus does not possess a maxillary sinus. Phylogenetic evaluation of the fossil with extant catarrhine taxa strongly supports the early loss of the sinus in cercopithecoids. The results suggest that the maxillary sinus found in the genus Macaca is not homologous with that of other eutherians, which may provide insights into the origin and function (if any) of the paranasal pneumatizations.

Animals↗

Long bone articular and diaphyseal structure in old world monkeys and apes. I: locomotor effects.

The relationship between locomotor behavior and long bone structural proportions is examined in 179 individuals and 13 species of hominoids and cercopithecoids. Articular surface areas, estimated from linear caliper measurements, and diaphyseal section moduli (strengths), determined from CT scans, were obtained for the femur, tibia, humerus, radius, and ulna. Both within-bone (articular to shaft) and between-bone (forelimb to hindlimb) proportions were calculated and compared between taxa. It was hypothesized that: 1) species emphasizing slow, cautious movement and/or more varied limb positioning (i.e., greater joint excursion) would exhibit larger articular to cross-sectional shaft proportions, and 2) species with more forelimb suspensory behavior would have relatively stronger/larger forelimbs, while those with more leaping would have relatively stronger/larger hindlimbs. The results of the analysis generally confirm both hypotheses. Several partial exceptions can be explained on the basis of more detailed structural-functional considerations. Associations between locomotion and structural proportions can be demonstrated both across major groupings (hominoids and cercopithecoids) and between relatively closely related taxa, e.g., mountain and lowland gorillas, siamangs and gibbons, and Trachypithecus and other colobines. Furthermore, structure and function do not always covary with taxonomy. For example, compared to cercopithecoids, mountain gorillas have relatively larger joints, like other hominoids, but do not have relatively stronger forelimbs, unlike other hominoids. This is consistent with a locomotor repertoire emphasizing relatively slow movement but with very little forelimb suspension. Proportions of Proconsul nyanzae, Proconsul heseloni, Morotopithecus bishopi, and Theropithecus oswaldi are compared with modern distributions to illustrate the application of the techniques to fossil taxa.

Animals↗