Craniometric sexual dimorphism inLeontopithecus Lesson, 1840 (Callitrichidae, Primates)

Lion tamarins are among the World's most critically endangered primates. Many studies have been produced under guidance of the International Management Committees for the preservation and management of these tamarins. Primates present morphological sexual differences in a wide range of characteristics, including cranial morphology. Studies of sexual dimorphism in the cranial morphology of theLeontopithecus are few in number and contradictory in their results. In order to check for the existence of sexual dimorphism in lion tamarins the present study analyzed 17 craniometric distances on 56 crania of three species of lion tamarins (Leontopithecus): 20L. rosalia (14 females and 6 males); 13L. chrysomelas (6 females and 7 males); and 23L. chrysopygus (8 females and 15 males). All crania are housed in the CPRJ-FEEMA collection (Primatological Center of Rio de Janeiro) and came from animals born in captivity.L. chrysopygus was more sexually dimorphic (10/17 measurements, 59%) thanL. chrysomelas (9/17 measurements, 53%) orL. rosalia (7/17 measurements, 41%). In all three species, male values are greater than the female ones, except for orbital breadth (m7) inL. rosalia. However, this distance is not sexually dimorphic in this species. This study reveals that some cranial distances, especially in the facial region, are sexually dimorphic in lion tamarins.     

Morphological variations of the cranium within the genusLeontopithecus

Multivariate analysis methods were applied to the cranial measurements ofLeontopithecus. InLeontopithecus chrysomelas, the face is generally narrow and the cranial shape is relatively unique. Especially, the male has extremely narrow face and quite unique cranial shape amongLeontopithecus. Leontopithecus rosalia has the broad face compared with the other species. The cranial size ofL. rosalia is as large as that ofL. chrysomelas. Male ofLeontopithecus chrysopygus is the largest in overall size of the cranium, and has the widest braincase.     

Examination of the Taxonomy and Diversification of <Emphasis Type="Italic">Leontopithecus</Emphasis> using the Mitochondrial Control Region

Leontopithecus comprises 4 taxa: black lion tamarins (L. chrysopygus), golden lion tamarins (L. rosalia), black-faced lion tamarins (L. caissara), and golden-headed lion tamarins (L. chrysomelas). Endemic to the Atlantic Forest of Brazil, they are endangered (Appendix I, CITES; IUCN Critically Endangered: Leontopithecus chrysopygus, L. caissara; IUCN Endangered: L. rosalia, L. chrysomelas). The 4 taxa are differentiated morphologically and geographically and occupy different habitat types. However, it is not clear if all of them are separate species, particularly Leontopithecus caissara, or how they are related to one another evolutionarily. Therefore, we investigated lion tamarin differentiation and radiation. We sequenced the mtDNA control region and performed phylogenetic analyses, population aggregation analyses, and Mantel tests for geographic/genetic correlation. Mitochondrial genetic data suggest 3 distinct lion tamarin clades (Leontopithecus chrysomelas; L. caissara; and L. chrysopygus/L. rosalia). Phylogenetic analysis also supports: 1) the basal lion tamarin is Leontopithecus chrysomelas, and not L. chrysopygus, 2) L. caissara is not subspecific to L. chrysopygus, and 3) Quaternary forest refugia may have shaped lion tamarin diversification via a pattern that does not follow the theory of metachromism. Even though mitochondrial genetic analyses do not unequivocally support the 4 lion tamarins as separate species, one should consider the 4 lion tamarins, with equal conservation priority based on the combination of morphological, genetic, and habitat differentiation. Each of them is an extremely valuable flagship species that focuses attention on the diminishing, highly endemic Atlantic Forest of Brazil.     

Long-call structure and its relation to taxonomy in lion tamarins

Recent evidence on craniodental morphology suggests the acceptance of three species of lion tamarins (Leontopithecus). Confirmatory evidence is presented here using the morphology of long-call vocalizations recorded from several individuals of each type of lion tamarin. Recordings were made of Leontopicthecus rosalia, Leontopithecus chrysopygus, and Leontopithecus chrysomelas at the Centro de Primatologia do Rio de Janeiro (FEEMA) and of L. rosalia at Monkey Jungle in Florida. Thirty separate parameters were measured, and 17 of them differed significantly between populations. In general, L. chrysomelas had higher pitched calls with shorter note duration, while L. chrysopygus, the larger of the animals, had lower pitched calls with longer note duration. L. rosalia was either intermediate to the other two populations or resembled L. chrysopygus. Thus, the results from the analysis of vocal structures closely paralleled the results obtained with more traditional taxonomic methods and suggests that the quantitative analysis of vocal strucures can be a useful adjunct in taxonomy.     

Distribution and ecology of the genusLeontopithecus lesson, 1840 in Brazil

The three forms of the genusLeontopithecus are found only in restricted localities in the States of Rio de Janeiro (Leontopithecus rosalia rosalia), Bahia and Espirito Santo (Leontopithecus rosalia chrysomelas) and São Paulo (Leontopithecus rosalia chrysopygus) in southeastern Brazil. All three are gravely threatened with extinction, mainly by destruction of primitive forest habitat. Diet ofLeontopithecus ssp. consists of fruit, buds, small vertebrates and insects. Group size varies from two to eight, but temporary congregations of up to 15–16 have been observed. Within the forest, the animals frequent the middle layers of the canopy, between three and ten meters above the ground.     

Reproduction in captive lion tamarins (Leontopithecus): Seasonality,infant survival,and sex ratios

Diversity in reproductive and social systems characterizes the primate family Callitrichidae. This paper contributes to our appreciation of this diversity by presenting the first detailed comparative analysis of captive breeding in three species of lion tamarins (Leontopithecus chrysomelas, L. chrysopygus, and L. rosalia) housed at the Centro de Primatologia do Rio de Janeiro. The annual pattern of reproduction in all three species of Leontopithecus was markedly seasonal, with births occurring during the spring, summer, and fall months from August through March. While modal number of litters produced per female per year was 1, approximately 20% of breeding females produced two litters per year. The onset of breeding activity in years when two litters are produced was significantly earlier than in years when only one litter was produced. The cumulative number of offspring surviving to 3 months of age did not differ between years with one vs. two breeding attempts. Like other callitrichids, postnatal mortality was highest during the first week of life, and there were pronounced species differences in offspring survival through 1 year, with significantly lower survivorship in L. chrysomelas. Infant survivorship was affected by a number of experiential factors. Survivorship up to 30 days of life was higher in groups in which the breeding female had previous experience with infants as a nonbreeding helper than in groups in which the female lacked previous helping experience. Likewise, survivorship to 30 days of life was higher for infants born to multiparous females than for infants born to primiparous females. When parity and previous helping experience were analyzed concurrently, the lowest survivorship was associated with offspring produced by inexperienced primiparous females. Genus-wide, there was no significant departure from a 50:50 sex ratio at any point during the first year of life, nor was there evidence for differential mortality for male and female infants. However, L. chrysopygus produced significantly more male infants at birth (65:44) and had male-biased litters (approximately 60% males) throughout the first year of life, while L. chrysomelas showed a nonsignificant tendency toward female-biased litters. © 1996 Wiley-Liss, Inc.     

Chromosomal similarities and differences between tamarins,Leontopithecusand Saguinus (Platyrrhini,Primates)

The karyotypes of two taxa of genus Leontopithecus(rosalia and chrysomelas) are studied. Their G-, C- and NOR-banding patterns are compared with those of representatives of the genus Saguinus to determine chromosomal similarities and differences between the two genera and thus contribute to explaining phylogenetic relations between the tamarins. Leontopithecus, like the Saguinus, presents 2n = 46, 14 autosomes plus the Y acrocentric and 30 autosomes plus the X biarmed. No chromosomal rearrangement distinguishes the karyotypes of the representatives of genus Leontopithecus or genus Saguinus. The two genera are distinguished from each other by a paracentric inversion and pericentric inversions on at least four pairs of acrocentric autosomes, displacing the NORs of the small short arms in Leontopithecus to the proximal region of the long arms in Saguinus or vice versa. The tamarins are also distinguished by the distribution of noncentromeric constitutive heterochromatin. The data obtained indicate that the two tamarin genera are closely related chromosomally, suggesting that they probably originated from the same ancestral branch. Am. J. Primatol. 43:265–276, 1997. © 1997 Wiley-Liss, Inc.     

Locomotion in captive Leontopithecus and Callimico: A multimedia study

Video studies, gait analysis, footprint tracks, and observational scan sampling show that, in comparably furnished enclosures, Leontopithecus rosalia and Callimico goeldii are superficially similar in their use of predefined locomotor patterns but differ profoundly in many underlying details which reflect differences in postcranial morphology. Each uses pronograde arboreal quadrupedal walking, quadrupedal bounding, and vertical climbing with comparable frequency, and both shift to bounding while moving quadrupedally at high speeds. In walking, both species use a diagonal sequence gait. However, in Callimico the distance per bout traveled while walking or running is shorter than in L. rosalia and there is an emphasis on leaping (from a stationary position) and bounding-leaps (saltational extensions of pronograde quadrupedalism), in contrast with the basically quadrupedal style of L. rosalia. This dichotomy is consistent with anatomical specializations, such as forelimb elongation in Leontopithecus and hindlimb elongation in Callimico. In vivo hand- and footprint studies demonstrate grasping halluces in both species while walking. Limb stances in L. rosalia during “transaxial bounding” involve an overstriding hindlimb, a predominance of oblique rather than in-line travel, and unique hand and foot positions. Anatomically, this locomotor style may be associated with reduced dexterity of the elongate hands and a relatively short hallux. The captive locomotor profiles for both species probably reflect biased samples of the locomotor repertoire of their wild counterparts. Nevertheless, these data reflect species-specific integrations of locomotor behavior and morphology, and corroborate expectations of locomotor diversity among callitrichine primates, even those of similar body size. It is suggested, however, that conventional quantitative studies of locomotor profiles may prove inadequate for resolving subtle aspects of locomotor morphology and behavior. © 1994 Wiley-Liss, Inc.     

Craniometric allometry in the thicktailed bushbabyOtolemur Crassicaudatus

Static adult craniometric allometry was evaluated in a sample of 66Otolemur crassicaudatus skulls (34 males, 32 females). Although cranial measures were equally well correlated to skull length in males and females, there were noteworthy differences in the exponential values between the sexes. These results underlined the need for caution when allometric analyses are based on pooled data. From the cranial allometric analyses it is concluded that the longer the skull, the shorter and the narrower the maxilla, and the broader the bizygomatic distance. Although cranial length increased proportionately to the increase in skull length, the cranial width in females was positively allometric whilst in males it was negatively allometric. Allometric analyses of mandibular dimensions suggest that larger animals will have proportionately longer mandibulae, which will, in turn, be relatively wider across the gonia, yet shallower behind the first molars. It is postulated that the disproportionate widening of the zygomata might be related to the widening across the gonia.     

Urinary and plasma gonadotropin concentrations in golden lion tamarins (Leontopithecus r. rosalia)

This paper describes the development and validation of a plasma and urinary gonadotropin immunoassay for golden lion tamarins (Leontopithecus rosalia), an endangered New World callitrichid primate. The assay is derived from a macaque chorionic gonadotropin assay and was validated for both plasma and urine samples in L. rosalia. Levels of immunoreactive LH/CG in lion tamarin urine were highly correlated (r = + 0.98) with gonadotropin bioactivity. Immunoreactive LH/CG levels were examined in two contexts: in the urine of adult females and in the plasma of adult males after administration of estrogen. Peaks of gonadotropin excretion were detected in samples collected from nonpregnant adult females. The peaks occurred immediately prior to cyclic elevations in urinary estrogen excretion. Plasma LH/CG concentration in males measured 24 and 48 hours after a single 50 μg injection of estradiol benzoate were significantly lower than levels at these time points measured after control treatment. Together, the results of this study point to the utility of the gonadotropin assay for monitoring reproductive function in both female and male lion tamarins.     

Pattern of late DNA replication of the allocyclic X chromosome in Cebus apella and Leontopithecus rosalia chrysomelas fibroblasts

The pattern of late DNA replication in the allocyclic X chromosome has been studied in the primary fibroblasts of two neotropical primates (Cebus apella and Leontopithecus rosalia chrysomelas). A comparison with previous reports showed a pattern identical with that of (1) the allocyclic X chromosome of human fibroblasts, and (2) the allocyclic X chromosome of rhesus and Cebus lymphocytes. Our results show that at least in one species (C. apella), and probably in rhesus and Leontopithecus, there is no tissue-specific difference between the late DNA replication patterns of the allocyclic X chromosome as there is between human lymphocytes and fibroblasts.     

Dinucleotide microsatellite primers designed for a critically endangered primate,the black lion tamarin (Leontopithecus chrysopygus)

Black lion tamarin (BLT) monkeys (Leontopithecus chrysopygus) have suffered a severe reduction in their natural range and are consequently critically endangered. Because allozyme data showed very low levels of variation, it was not clear if these monkeys had much genetic diversity. We designed microsatellite primers for BLTs, and from them we identified nine polymorphic loci, seven of which were tested on golden lion tamarins (GLTs) (Leontopithecus rosalia). All of the seven polymorphic loci and two other monomorphic BLT loci were polymorphic in GLTs. The microsatellite markers identified here are directly applicable to ongoing lion tamarin population and conservation genetics studies.     

Mandible/basihyal relationships in red howler monkeys (Alouatta seniculus): A craniometrical approach

The morphological relationships between the cranium and basihyal of red howler monkeys (Alouatta seniculus) were analyzed based on measurements of 36 cranial and 3 basihyal dimensions and observations of the female specimen in spirits. In this study, 115 crania from 111 red howler monkeys and 4 mantled howler monkeys (Alouatta palliata) were used. The analyses from the standpoints of the correlation coefficients, principal component analysis, discriminant function analysis, age changes and sex differences were performed and the following results were obtained: (1) The cranial measurements closely related to the basihyal measurements were mandibular length, occipital breadth, facial length, ramus height, cranial base length, bigonial breadth and pr-i length. (2) Age changes for the mandibular measurements in males of red howler monkeys were remarkable, and, in particular, the development of the gonion toward posterior and lateral directions were characteristic. (3) The largest sex differences were found in the mandibular measurements of red howler monkeys among the Anthropoidea of seven genera compared. (4) The existence of a “cline” in the cranial measurements of the red howler monkey was recognized. (5) The inter-species differences in the crania between the red howler monkey and mantled howler monkey are obvious, metrically and non-metrically. Based on the results mentioned above, the morphological relationships between the mandible and basihyal in the red howler monkey are discussed.     

Strength of Habitat and Landscape Metrics in Predicting Golden-Headed Lion Tamarin Presence or Absence in Forest Patches in Southern Bahia,Brazil

We investigated the effects of forest fragmentation on golden-headed lion tamarins (Leontopithecus chrysomelas) by qualitatively and quantitatively characterizing the landscape throughout the species range, conducting surveys, and exploring predictive models of presence and absence. We identified 784 forest patches that varied in size, shape, core area, habitat composition, elevation, and distance to neighboring patches and towns. We conducted 284 interviews with local residents and 133 playback experiments in 98 patches. Results indicated a reduction in the western portions of the former species range. We tested whether L. chrysomelas presence or absence was related to the aforementioned fragmentation indices using Monte Carlo logistic regression techniques. The analysis yielded a majority of iterations with a one-term final model of which Core Area Index (percent of total area that is core) was the only significant type. Model concordance ranged between 65 and 90 percent. Area was highlighted for its potential predictive ability. Although final models for area lacked significance, their failure to reach significance was marginal and we discuss potential confounding factors weakening the term's predictive ability. We conclude that lower Core Area Index scores are useful indicators of forest patches at risk for not supporting L. chrysomelas. Taken together, our analyses of the landscape, survey results, and logistic regression modeling indicated that the L. chrysomelas metapopulation is facing substantial threat. The limited vagility of lion tamarins in nonforest matrix may lead to increasingly smaller and inbred populations subject to significant impact from edge effects and small population size. Local extinction is imminent in many forest patches in the L. chrysomelas range.     

Morphological analysis ofAlouatta seniculus species group (Primates,Cebidae). A comparison with biochemical and karyological data

Fifteen cranial measurements were taken from wild caught specimens ofAlouatta seniculus seniculus, A. s. stramineus andA. s. macconnelli. A morphological analysis showed sex dimorphism in these three groups. A multivariate analysis discriminated among these taxa; males being more clearly discriminated than females. Our data showed that these taxa can be separated on the basis of quantitative cranial traits, biogeographic distribution, karyological differences, and biochemical characters. We therefore propose a new taxonomic arrangement, changing their taxonomic status to the species level (Alouatta seniculus, A. macconnelli, andA. stramineus).     

A morphometric analysis of the Japanese macaque (Macaca fuscata) mandibular cheek teeth from the Torihama Shell-midden, Early Jomon Period, Fukui Prefecture, Japan

We quantitatively examined the differences in the size and proportion of the Japanese macaque (Macaca fuscata) by comparing the Early Jomon specimens from Torihama shell-midden, Fukui Prefecture and modern specimens from Fukui Prefecture. The purpose of this study was to explore the temporal change in the proportion and size of teeth of the Japanese macaques based on the quantified data. The result of measurements of lower premolars and molars demonstrated that sexual dimorphism was evident only among the modern specimens where the females were significantly smaller than males. The size of male Torihama specimens was within the range of the modern population, whereas the size of the female Torihama specimens was significantly larger than the modern female population. The proportional pattern of premolars and molars for male and female Torihama specimens also differed. The results may suggest a possible difference in the degree of size reduction between males and females since the last glacial period.Morphometric analysis of mandibular cheek teeth from Torihama Shell-midden     

The cranial and cervical osteology of the european oystercatcher Haematopus ostralegus L.

The cranial and cervical osteology of the European oystercatcher, Haematopus ostralegus L. is completely described from both whole skeletons and spirit specimens. Contrary to previous reports, the postorbital ligament shows variability in bifurcation and attachment, with the posterior branch, where present, attaching either to the suprameatic process or the zygomatic process. In addition, the quadrate ligament, which had been described as originating from the suprameatic process, appears instead to attach to the zygomatic process in some specimens. The caudal mandibular fenestra, earlier considered absent in oystercatchers, is present in all specimens examined. The cranium is additionally distinguished by a number of features which may be unique to oystercatchers. A fourth, previously unrecorded, division of the maxillopalatine strut is present, while the palatine process of the premaxilla is reduced to a thickening along the edge of the premaxillary process of the palatine. The distinctiveness of the oystercatcher cranium is particularly evident in the area of the quadratomandibular articulation, which possesses features potentially important for stabilizing the joint. A deep retroarticular notch is present, guiding a large medial jugomandibular ligament along the posterior margin of the articulation. A lateral mandibular tuberosity, which is received dorsally by an emargination of the jugal arch and quadrate, may act as an osteological brace, preventing posterior shifting of the closed mandible. The 15 cervical vertebrae are divided on the basis of structural criteria into three sections.     

Proposed chromosomal phylogeny for the South American primates of the Callitrichidae family (Platyrrhini)

Cytogenetic and cytotaxonomic studies (G, C, sequential G/C, and NOR banding) were performed on 110 specimens representing the four genera of South American primates of the family Callitrichidae: Cebuella (C. pygmaea), Callithrix, groups argentata (C. argentata, C. emiliae, C. chrysoleuca, C. humeralifera, C. mauesi), and jacchus (C. aurita, C. geoffroyi, C. jacchus, C. kuhli, C. penicillata), Leontopithecus (L. chrysomelas, L. rosalia), and Saguinus (S. midas midas, S. m. niger). Mitotic chromosomes are characterized, and the rearrangements distinguishing the karyotypes of the taxa are inferred from arm homologies. The results were then converted into numerical data and submitted to cladistic analysis. The following conclusions were achieved: 1) Five karyotypic classes were observed, which correspond to the five taxa studied. Differences between them are as follows: a) Cebuella (2n = 44, 10 acrocentrics, A + 32 bi‐armed autosomes, bi) and the argentata group (2n = 44, 10A + 32bi) are different from each other due to a reciprocal translocation; b) both can be distinguished from the jacchus group (2n = 46, 14A + 30bi) by a centric fusion/fission rearrangement and a paracentric inversion; c) Leontopithecus (2n = 46, 14A + 30bi) and Saguinus (2n = 46, 14A + 30bi) differ from the jacchus group by a reciprocal translocation and three paracentric inversions; and d) Saguinus is different from the others by one paracentric inversion and pericentric inversions in at least four pairs of acrocentric autosomes. 2) The cladistic analysis separates Cebus (used as an outgroup) from the Callitrichidae groups, which forms a clade. Among the Callitrichidae, marmosets (Cebuella and Callithrix) form a sub‐clade, Cebuella and the argentata group being more closely related to each other than both are to the jacchus group. Tamarins (Leontopithecus and Saguinus) are also quite close, so that if one was not derived from the other, they with the marmosets share a common ancestor. Among the tamarins, Leontopithecus is karyotypically closest to the marmosets, specifically to the jacchus group. 3) Based on the chromosome information and considering the possible direction of the evolutionary changes (primitivity or phyletic dwarfism hypothesis, previously advanced by other authors), it was possible to propose the ancestral karyotypes and to develop two alternatives for the origin, differentiation and dispersion of the callitrichid. Both proposals are plausible, but when the geographical distribution is considered, the phyletic dwarfism hypothesis seems to be the most probable. Am. J. Primatol. 49:133–152, 1999. © 1999 Wiley‐Liss, Inc.     

Morphological variation in adult chimpanzees (Pan troglodytes verus) of the Taï National Park, Côte d'Ivoire

Twenty five adult chimpanzee skeletons (Pan troglodytes verus) of known age and sex (15 females, 10 males) from a long‐term study site in Taï National Park, Cote d'Ivoire present new data on variation. These skeletons provide a rare opportunity to measure the cranium and postcranium from the same individuals. We compare measurements and indices of the Taï sample with those of relatively complete Pan troglodytes schweinfurthii skeletons from Gombe National Park, Tanzania. Measurements of Pan paniscus are included as an outside comparison. The Taï and Gombe samples are analyzed by sex; combined sex samples are compared between the two groups, and the two sexes to each other. Taï females and males do not differ in most long bone lengths or in pelvic dimensions, but do differ significantly in cranial capacity, facial measurements, clavicle length, scapular breadth, and femur length. Gombe females and males differ significantly in some facial measurements and in scapular breadth. In combined sex samples, Taï individuals have lower cranial capacity, longer palate and mandible, and greater dimensions in the trunk and limb lengths. Taï females account for most of the variation; males differ from each other only in greater length of humerus and femur. The Taï skeletons provide new data for assessing individual variation and sexual dimorphism within and between populations and species. The combination of cranial and postcranial data provides a clearer picture of chimpanzee intraspecific and interspecific variation than can be gained from either data set alone. Am J Phys Anthropol, 2008. © 2007 Wiley‐Liss, Inc.     

Sexual dimorphism in the skull geometry of newt species of <Emphasis Type="Italic">Ichthyosaura,Triturus</Emphasis> and <Emphasis Type="Italic">Lissotriton</Emphasis> (Salamandridae,Caudata, Amphibia)

In this study, we applied geometric morphometrics to explore variations in the level and pattern of sexual size dimorphism (SSD) and sexual shape dimorphism (SShD) of the ventral cranium in three different Modern Eurasian newt taxa (Ichthyosaura alpestris, Triturus species group and Lissotriton vulgaris). The ventral cranium is the part of the skull that is more directly related to foraging and feeding. Our results indicate that the level and pattern of sexual dimorphism in the ventral cranium differ among Modern Eurasian newt taxa. Regarding sexual dimorphism in skull size, Ichthyosaura alpestris and Triturus species show female-biased patterns (females are larger than males), whereas Lissotriton vulgaris appears to be non-dimorphic in skull size. In I. alpestris and Triturus species, SShD is mostly absent, whereas in L. vulgaris, SShD is more pronounced. A high level of variation between populations in both SSD and SShD indicates that local conditions may have a profound effect on the magnitude and direction of sexual dimorphism. The significant sexual differences in ventral cranium size and shape indicate possible subtle intersexual differences in ecological demands due to diet specialisation, in spite of similar general ecological settings.