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Accessory chemosignaling mechanisms in primates.

Accessory olfaction is defined as the chemoreceptive system that employs the vomeronasal complex (VNC) and its distinct central projections to the accessory olfactory bulb (AOB) and limbic/cortical systems. Comparisons of the structural and functional features of primate accessory olfaction can now be made at many levels. Advances in the understanding of molecular mechanisms of odorant transfer and detection, physiological analyses of signal processing, and appreciation of ontogenetic timetables have clarified the contribution of accessory chemoreception to the sensory map. Two principal functions dominate: the decoding of social information through the uptake of signals (often fluid-borne), and the provision of an essential pathway for the "migration" of presumptive neurocrine (GnRH) cells from the olfactory placode to the hypothalamus. VN "smelling" (vomerolfaction) is now seen to overlap with primary olfaction. Both systems detect signal compounds along the spectrum of volatility/molecular weight, and neither is an exclusive sensor. Both main and accessory chemoreception seem to require collaborative molecular devices to assist in odorant transfer (binding proteins) and (for the VNO) signal recognition (MHC1 proteins). Most adaptive-selective features of primate chemocommunication variously resemble those of other terrestrial mammals. VN function, along with its genome, has been maintained within the Strepsirrhines and tarsiers, reduced in Platyrrhines, and nearly extinguished at the Catarrhine up to hominin levels. It persists as an intriguing ancient sense that retains key features of past evolutionary events.

Animals↗

The importance of ingestion rates for estimating food quality and energy intake.

Testing ecological or socioecological models in primatology often requires estimates of individual energy intake. It is a well established fact that the nutrient content (and hence the energy content) of primate food items is highly variable. The second variable in determining primate energy intake, i.e., the ingestion rate, has often been ignored, and few studies have attempted to estimate the relative importance of the two predictors. In the present study individual ingestion rates were measured in two ecologically very different populations of Hanuman langurs (Semnopithecus entellus) at Jodhpur, India, and Ramnagar, Nepal. Protein and soluble sugar concentrations in 50 and 100 food items. respectively, were measured using standardized methods. Variation in ingestion rates (gram of dry matter per minute) was markedly greater among food items than among langur individuals in both populations, but did not differ systematically among food item categories defined according to plant part and age. General linear models (GLMs) with ingestion rate, protein, and soluble sugar content explained 40-80% of the variation in energy intake rates (kJ/min). The relative importance of ingestion rates was either similar (Ramnagar) or much greater (Jodhpur) than the role of sugar and/or protein content in determining the energy intake rates of different items. These results may impact socioecological studies of variation in individual energy budgets, investigations of food choice in relation to chemical composition or sensory characteristics, and research into habitat preferences that measures habitat quality in terms of abundance of important food sources. We suggest a definition of food quality that includes not only the amount of valuable food contents (energy, vitamins, and minerals) and the digestibility of different foods, but also the rate at which the food can be harvested and processed. Such an extended definition seems necessary because time may constrain primates when feeding competition is intense and foraging is risk-prone.

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Perceptual considerations in the use of colored photographic and video stimuli to study nonhuman primate behavior.

The use of photographs, slides, computerized images, and video to study behavior is increasingly being employed in nonhuman primates. However, since these mediums have been designed to simulate natural coloration for normal trichromatic human vision, they can fail to reproduce color in meaningful and accurate ways for viewers with different visual systems. Given the range of color perception that exists both across and within different species, it is necessary to consider this variation in order to discern the suitability of these mediums for experimental use. Because of the high degree of visual similarity among humans, Old World monkeys, and apes, the use of photographic and video stimuli should be acceptable in terms of replicating naturalistic coloration and making noticeable color manipulations. However, among New World primates and prosimians, there exists a considerable degree of variation in color perceptual abilities depending on the species, sex, and allelic combination of the animals involved. Therefore, the use of these mediums to study behavior is problematic for these species, and should be done with caution.

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Genital swellings in silvered langurs: what do they indicate?

The occurrence of genital swellings was examined in adult female silvered langurs (Trachypithecus cristatus). In contrast to the exaggerated swellings found in cercopithecines and apes, genital swellings in silvered langurs are confined to the vulva and the surrounding perineum, but they may nevertheless convey information similar to that of exaggerated swellings (i.e., correlate with the receptive period and fertility). If so, genital swellings would be expected to occur most frequently in cycling females, and sexual behavior and male interest should most frequently involve females with swellings. Swellings during gestation, if they occur at all, should be most pronounced at the beginning. Swelling sizes (in three size categories) in nine adult females were examined throughout different reproductive states (cycling, pregnant, and lactating), and in relation to proceptivity, receptivity, and attractivity. Data were collected from November 2002 through March 2004 (on 500 of the 502 calendar days) at the Wildlife Conservation Society's Bronx Zoo. Female sexual behavior (proceptivity and receptivity) and male inspection (attractivity) were recorded each day for 6 hr by video camera (2,948 hr total) and analyzed as present or absent for each female day. Swellings were assessed directly (not from videotapes). In contrast to the predictions, swellings occurred significantly less frequently in cycling females (compared to pregnant females) and no regular, cyclic pattern could be detected. Some females conceived without a swelling. Female attractivity was independent of swellings but coincided with proceptive behavior. Swellings occurred most frequently in pregnant females, especially toward the end of the gestation period. Therefore, genital swellings in silvered langurs are not similar to exaggerated swellings or the smaller genital swellings that have been described for some other primates. It is currently not clear what they signal to conspecifics. Male behavior needs to be studied in more detail, and the hormonal basis for these swellings should be explored.

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Demography and life history of Thomas langurs (Presbytis thomasi).

Life history data from wild primate populations are necessary to explain variation in primate social systems and explain differences between primates and other mammals. Here we report life history data from a 12.5-year study on wild Thomas langurs. Mean age at first reproduction was 5.4 years and the sex ratio at birth was even. The mean interbirth interval (IBI) after a surviving infant was 26.8 mo, after nonsurviving infants 17.7 mo, and combined 22.0 mo. Mean annual birth rate of adult females was 0.44, while reaching a peak at 6 years of age and showing no decrease with age. Mortality was highest during the first year of life (48.0% for males and 43.0% for females) and consistently higher for males than females. The oldest female observed during the study was estimated to be 20 years of age, whereas the oldest male disappeared at age 13 years, indicating that males die at a much earlier age than females. A Leslie matrix based on these estimates yielded a growth rate of 1.01, which is comparable to the nonsignificant increase in density indicated by our long-term field data. A comparison with life history data for sympatric frugivorous primates suggests that folivory might be associated with faster life history.

Age Factors↗

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.

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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.

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Long bone articular and diaphyseal structure in Old World monkeys and apes. II: Estimation of body mass.

Body mass estimation equations are generated from long bone cross-sectional diaphyseal and articular surface dimensions in 176 individuals and 12 species of hominoids and cercopithecoids. A series of comparisons is carried out to determine the best body mass predictors for each of several taxonomic/locomotor groupings. Articular breadths are better predictors than articular surface areas, while cross-sectional shaft strengths are better predictors than shaft external breadths. Percent standard errors of estimate (%SEEs) and percent prediction errors for most of the better predictors range between 10-20%. Confidence intervals of equations using sex/species means are fairly representative of those calculated using individual data, except for sex/species means equations with very low %SEEs (under about 10%), where confidence intervals (CIs) based on individuals are likely to be larger. Given individual variability, or biological "error," this may represent a lower limit of precision in estimating individual body masses. In general, it is much more preferable to determine at least broad locomotor affinities, and thus appropriate modern reference groups, before applying body mass estimation equations. However, some structural dimensions are less sensitive to locomotor distinctions than others; for example, proximal tibial articular M-L breadth is apparently "locomotor blind" regarding body mass estimation within the present study sample. In other cases where locomotor affiliation is uncertain, mean estimates from different reference groups can be used, while for some dimensions no estimation should be attempted. The techniques are illustrated by estimating the body masses of four fossil anthropoid specimens of Proconsul nyanzae, Proconsul heseloni, Morotopithecus bishopi, and Theropithecus oswaldi.

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Taxonomic affinities of the Eppelsheim femur.

The taxonomic affinities of the Eppelsheim femur, known as Paidopithex, have been unclear for more than a century. Over the years, due to similarities with Pliopithecus, some authors have considered it a large pliopithecid, while others refer to it as Dryopithecus. The issue could not be resolved, because no definitive Dryopithecus femora were available. With the discovery of the Dryopithecus laietanus skeleton from Can Llobateres (CLl 18800), it has become possible to test the attribution of the Eppelsheim femur to Dryopithecus on the basis of direct morphological and metrical comparisons. By means of allometric techniques, we show that the Eppelsheim and D. laietanus femora fit different hindlimb morphologies with regard to relative length and relative head/neck size, with Paidopithex significantly differing from Dryopithecus, but more closely resembling Pliopithecus. Paidopithex also differs from Dryopithecus in other important aspects, such as its lower neck/shaft angle, lack of elevation of the femoral head above the greater trochanter, more posteriorly oriented lesser trochanter, and proximal shaft diameter thicker anteroposteriorly than mediolaterally. In these features, Paidopithex most closely resembles Pliopithecus in spite of differences in body mass (ca. 22 kg vs. ca. 10 kg, respectively). These features suggest that Paidopithex used a primitive locomotor pattern associated with arboreal quadrupedalism, instead of the more derived pattern displayed by Dryopithecus. Currently available evidence confirms that the attribution of Paidopithex to Dryopithecus can be rejected. Paidopithex could be a large and otherwise unknown pliopithecid, but the possibility cannot be ruled out that it represents a third kind of catarrhine.

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Integration, phylogeny, and the hominid cranial base.

Basicranial features were examined in catarrhine primates and early hominids in order to demonstrate how information about morphological integration can be incorporated into phylogenetic analysis. Hypotheses purporting to explain the functional and structural relationships of basicranial characters were tested using factor analysis. Characters found to be functionally or structurally related to each other were then further examined in order to determine whether there was evidence that they were phylogenetically independent. If phylogenetic independence could not be demonstrated, then the characters were presumed to be integrated and were grouped into a complex. That complex was then treated as if it were a single character for the purposes of cladistic analysis. Factor analysis revealed that five basicranial features may be structurally related to relative brain size in hominoids. Depending on how one defines phylogenetic independence, as few as two, or as many as all of those characters might be morphologically integrated. A cladistic analysis of early hominids based on basicranial features revealed that the use of integrated complexes had a substantial effect on the phylogenetic position of Australopithecus africanus, a species whose relationships are poorly resolved. Moreover, the use of complexes also had an effect on reanalyses of certain published cladistic data sets, implying that those studies might have been biased by patterns of basicranial integration. These results demonstrate that patterns of morphological integration need to be considered carefully in all morphology-based cladistic analyses, regardless of taxon or anatomical focus. However, an important caveat is that the functional and structural hypotheses tested here predicted much higher degrees of integration than were observed. This result warns strongly that hypotheses of integration must be tested before they can be adequately employed in phylogenetic analysis. The uncritical acceptance of an untested hypothesis of integration is likely to be as disruptive to a cladistic analysis as when integration is ignored.

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Egarapithecus narcisoi, a new genus of Pliopithecidae (primates, catarrhini) from the Late Miocene of Spain.

Pliopithecid remains from the Spanish locality of Torrent de Febulines (Late Vallesian, MN 10), consisting of right and left mandibular fragments with partial tooth rows and an isolated P(3) probably belonging to the same individual, are described and assigned to Egarapithecus narcisoi gen. et sp. nov. (Pliopithecidae, Crouzeliinae). This is a highly derived species dated at around 9 Ma (Ma = 10(6) years), representing the latest appearance of the family in the European continent. Morphologically it is the most distant member from the inferred primitive pliopithecid morphotype, displaying many autapomorphies that notably accentuate those of the remaining Crouzeliinae. A cladistic analysis based on lower cheek teeth, performed in order to tentatively assess the phylogenetic relationships of Egarapithecus within the Crouzeliinae, indicates that several equally parsimonious cladograms are possible in the light of current evidence. This is due to uncertainties regarding the position of Plesiopliopithecus and Crouzelia (here considered distinct genera), as a result of missing characters and the significant degree of homoplasy apparently involved in crouzeliine dental evolution. Whether Egarapithecus is more closely related to Crouzelia or to Anapithecus (the latter hypothesis tentatively favored here) cannot be definitively resolved with the currently available material and deserves further investigation. It is clear, however, that Egarapithecus is one of the more derived and specialized members of the Pliopithecidae.

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Allometry of primate hair density and the evolution of human hairlessness.

Allometric analyses of hair densities in 23 anthropoid primate taxa reveal that increasingly massive primates have systematically fewer hairs per equal unit of body surface. Considering the absence of effective sweating in monkeys and apes, the negative allometry of relative hair density may represent an architectural adaptation to thermal constraints imposed by the decreasing ratios of surface area to volume in progressively massive primates. Judging by estimates of body volume, denudation of the earliest hominids should have progressed to a considerable extent prior to their shift from a forest to a grassland habitat during the Pliocene. We propose that, lacking a reflective coat of hair, the exploitation of eccrine sweating emerged as the primary mechanism for adaptation to the increased heat leads of man's new environment and permitted further reduction of the remnant coat to its present vestigial condition.

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Sexual dimorphism and allometry in primate ossa coxae.

Five measurements were taken on the ossa coxae of 454 adult primates representing Ceboidea, Cercopithecoidea and Hominoidea. Sex differences in these variables and their relationships to overall body size and sexual dimorphism were tested by means of Student's T-test and regression analysis. The study attempts to clarify the nature of primate pelvic sexual dimorphism, including allometric effects, and more specifically, test the assertion made by Mobb and Wood (1977) that sexual dimorphism in body size in not an important determinant in pelvic sex differences. Variables that contribute to the size of the birth canal tend to be larger in females than males in all taxa studied except two. In these, Hylobates and Alouatta, there were no significant differences between the sexes for any of the five variables. In general, sexual dimorphism in variables contributing to the size of the birth canal was correlated (r approximately or equal to 0.8) with sexual dimorphism in body size. Furthermore, the coefficients of allometry underlying pelvic sex differences were shown to be moderately correlated (r approximately or equal to 0.5) with sexual dimorphism in size. The influence of other adaptive factors on primate pelvic sexual dimorphism are also briefly discussed.

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The morphology and wear of the lingual notch in macaques and langurs.

Although interspecific differences in the relative development of molar occlusal features have been documented for most primate species, wear-related changes in these features are only beginning to be understood. In the present study, the notch between the metaconid and entoconid of M2 was examined in a skeletal sample of Macaca fascicularis, presbytis cristatus, and Presbytis rubicunda from the Museum of Comparative Zoology at Harvard University. Photogrammetric analyses yielded X, Y, and Z coordinates that were used to compute three angular measurements and two length measurements at the lingual notch. Statistical analyses of measurements from unworn dentitions indicated that the mesial slope of the entoconid is steeper than the distal slope of the metaconid in all three species. In addition, interspecific comparisons demonstrated that P. cristatus has the steepest lingual notch bordered by the largest molar shearing crests, while P. rubicunda and M. fascicularis have molar shearing crests of similar size, with P. rubicunda merely having higher cusps that are closer together than those of M. fascicularis. Finally, P. cristatus shows a smaller decrease in lingual cusp relief with wear than M. fascicularis, while P. cristatus and P. rubicunda probably show similar decreases in lingual cusp relief with wear. The differences in wear-related changes in lingual cusp relief between M. fascicularis and P. cristatus may well be related to the frugivorous/folivorous dietary differences between these species.

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Ontogenetic and interspecific organ weight allometry in Old World monkeys.

The importance of allometry as an analytic tool is well recognized in the literature of primate morphology. However, a number of recent studies have illustrated how interpretive difficulties can arise when researchers confound different types of allometric data. Such confusion is due less to carelessness than to uncertainty about how different types of allometry are related. The present study examines the relationship between two types--ontogenetic and interspecific allometry--in the case of organ weight scaling in six species of Old World monkeys. Accepting the interpretation of interspecific allometry as a reflection of functional scaling constraints, the results of this analysis indicate how ontogenetic patterns have been modified in different-sized species to maintain compliance with these constraints. Specifically, for the heart and lungs it appears that vertical transpositions of individual species' ontogenies are dictated by isometric interspecific allometry, while in the case of the kidneys and liver, the relation of negative allometry across species entails alteration of the relative growth coefficients of the individual species. While these conclusions can at present only be applied to organ weight scaling, the approach of examining interspecific patterns in light of developmental differences between species should prove very helpful in our efforts to understand the phenomena of size and scaling.

Aging↗