An analysis of interspecific relationships ofSaguinus based on cranial measurements

The interspecific relationships of the following nine forms ofSaguinus were analyzed applying the multivariate analysis to the cranial measurements;S. oedipus, S. geoffroyi, S. leucopus, S. nigricollis, S. fuscicollis, S. labiatus, S. mystax, S. midas midas, andS. midas niger. Penrose's size distance was used to express the size factor among the nine forms; and for the shape factor, Q-mode correlation coefficients were utilized. The shape distance betweenS. oedipus andS. geoffroyi was almost equal to that betweenS. nigricollis andS. fuscicollis which are recognized as different species based on biogeographical evidence. Furthermore, the Penrose's size distance betweenS. oedipus andS. geoffroyi was quite large. Therefore, the results of this study support the hypothesis thatS. oedipus andS. geoffroyi are valid species. The analysis of the phylogenetic relationships among the nine forms was based on the shape factor only. The forms were divided into two main clusters: (1)S. oedipus, S. geoffroyi, andS. leucopus; (2)S. nigricollis, S. fuscicollis, S. labiatus, S. mystax, S. midas midas, andS. midas niger. In the former cluster,S. oedipus was more closely related toS. geoffroyi than either was toS. leucopus. The latter cluster was subdivided in two subclusters based on the degree of their affinity: (2a)S. nigricollis, S. fuscicollis, S. labiatus, andS. mystax; and (2b)S. midas midas andS. midas niger. In the former subcluster, [S. nigricollis, S. fuscicollis] and [S. labiatus, S. mystax] were classified into clusters, respectively. The ancestor of theS. nigricollis group differentiated intoS. oedipus, S. geoffroyi, andS. leucopus with the narrowing of the maxilla in the facial region, andS. midas midas andS. midas niger with the downward movement of rhinion.     

Preliminary analysis of numerical taxonomy of the genusSaguinus based on dental measurements

Although several investigations have been made from different viewpoints, the classification or interspecific relationships ofSaguinus still remain uncertain. In the present study, we applied multivariate analysis methods to dental measurements of part ofSaguinus populations of sufficient sample size and obtained the following conclusions.Saguinus can be classified into two main groups: one consists ofS. oedipus andS. leucopus, and the other ofS. fuscicollis, S. nigricollis, S. labiatus, andS. mystax. Concerning the former group, the two subspecies ofS. oedipus, S. o. oedipus, andS. o. geoffroyi, show a close affinity with each other and also a close relationship toS. leucopus, while the latter group consists of two subgroups of species, one includingS. fuscicollis andS. nigricollis, and the other includingS. labiatus andS. mystax. The biological distance betweenS. oedipus oedipus andS. o. geoffroyi is slightly larger than that between the pairs ofS. fuscicollis andS. nigricollis and ofS. labiatus andS. mystax. Factor analysis revealed significant factors which could explain the differences among the seven maleSaguinus populations. Taking all the results into account, it seems necessary to reconsider the phylogenetic relationships within the genusSaguinus.     

Numerical analysis of sexual dimorphism inSaguinus dentition

Among New World monkeys, more or less sexual dimorphism exists in the dentition, especially in the Cebidae. On the other hand, the Callitrichidae includingSaguinus are said to be characterized by a broad lack of sexual dimorphism with the exception of the reproductive organs. In the present article, sexual dimorphism in the dentition of someSaguinus species was reconfirmed using univariate and multivariate analytical methods. The results of the analysis were as follows: (1) there is no sexual dimorphism in the canine tooth size, except for the upper canine ofS. geoffroyi and lower canine ofS. mystax; (2) the overall tooth size difference between males and females is slight or none inS. geoffroyi, S. leucopus, andS. fuscicollis, relatively small inS. oedipus andS. mystax, and rather larger inS. midas; (3) an overall difference in shape factor between both sexes exists in all species ofSaguinus to a greater or lesser extent; (4) although only slight sexual dimorphism is recognized in the canine tooth itself, sexual dimorphism does exist in some adjacent teeth of the canine in a few species; and (5) there are some interspecific differences in the magnitude of the sexual dimorphism of theSaguinus dentition and these differences are more evident in species inhabiting the peripheral regions of the distribution areas of this genus. Taking all the evidence obtained into account, the sexual dimorphism in theSaguinus dentition must be re-investigated in comparison with other genera of the Callitrichidae.     

A comparative study of positional behavior in three species of tamarin monkeys

Tamarins of the genusSaguinus are small-bodied New World monkeys that exhibit clawlike or modified nails. Patterns of positional behavior and habitat utilization are presented for three species,Saguinus fuscicollis, S. geoffroy, andS. mystax. These data were collected on free-ranging tamarin populations in Panama and Peru. Despite considerable differences in body weight, all three species exhibited very similar patterns of positional behavior, with quadrupedal bounding and running accounting for 43 – 52% of travel time. Leaping was the second most common locomotor activity and accounted for 31 – 41% of travel. Although each species leaped principally on small supports in the perimeter of the tree crown, approximately 20% of all leaps inS. fuscicollis involved moderate to large sized vertical trunks located in the undercanopy. Leaping between trunks was rare in the two larger tamarin species. Measurements taken on live wild-trapped adults reveal that compared toSaguinus geoffroyi andS. mystax, S. fuscicollis is characterized by a long legspan and an especially long armspan. It is proposed that inS. fuscicollis, elongated forelimbs play an important role in maneuvering and rotating the body during the in-air phase of trunk-to-trunk leaping, and increase the breaking distance needed to decelerate the body upon impact. Additional relationships between body size, substrate preference, and positional behavior in callitrichines are discussed.     

Biochemical diversity and genetic distance in two species of the genusSaguinus

A comparative study of 20 blood genetic systems was performed on three populations of genusSaguinus: S. fuscicollis weddelli, S. midas niger, andS. midas midas. Some markers are useful for the characterization of the two species.ADA ⁵, ADA⁶, CA2³, CA2⁴, andES2 ² occur only inS. fuscicollis whileADA ⁴is fixed inS. midas. S. midas midas showed heterozygosity value comparable to those previously obtained for the genusAlouatta. Estimates of genetic distance betweenS. fuscicollis andS. midas species of about 14% are in accordance with those referred to in the literature for interspecific differences. Genetic distances between subspecies ofSaguinus midas were nearly 3%, which is within the range for subspecies.     

Fine structure of the dental enamel in the Family Callitrichidae (Ceboidea,primates)

The fine structure of the dental enamel was intensively examined in the Family Callitrichidae.Leontopithecus rosalia has the nonserial pattern, butCallimico goeldii andSaguinus midas appear more or less modified from the typical nonserial pattern asSaimiri sciureus has (see Figs. 1 & 5). On the other hand,Callithrix jacchus andCebuella pygmaea attain to the primitive stage of the multiserial pattern (see Figs. 4 & 6). So far as the structural patterns of the dental enamel are concerned, a serial trend is confirmed in the Callitrichidae; extending from the genusLeontopithecus through the generaCallimico andSaguinus to the generaCallithrix andCebuella. The genusSaguinus shows extremely wide interspecific variation in the fine structure of the dental enamel, ranging fromS. leucopus with the most primitive features toS. bicolor with the most advanced (see Figs. 2 & 3). The rows of enamel prisms are slightly twisted mesiodistally in the former species, but strongly folded in the latter. This reflects transitional stages from the nonserial pattern to the multiserial. As a whole, however, the genusSaguinus is still regarded as nonserial. Thus, there is a slight, but important gap between the genusSaguinus andCallithrix, as shown by the decussation of clusters (see Fig. 5), as well as by other characters.     

Reduction index of the upper M2 in marmosets

Marmosets have reduced second molars of which size and shape are varied in different species. Mesiodistal and buccolingual diameter of the first and second upper molars in 16 species were measured, and molar area (molar rectangle) and M2 reduction index were calculated by the equation,R=(M2 area/M1 area) × 100. This index ranged from 36.1 inSaguinus oedipus geoffroyi to 70.6 which was the largest found inCebuella pygmaea. Species ofSaguinus showed relatively wide variation as well as a consistantly smaller index. The index forCallithrix registered around 60 andLeontopithecus rosalia was positioned within this genus. There was no relationship between this index and body size of each form. The sizes of the first molar and second molar may not significantly correlate either with body size across species, becauseLeontopithecus rosalia had exceptionally large molars for its body size and contrarily genusSaguinus had relatively small molars. When the shape of the mandible was expressed as length/width ratio, the reduction index significantly correlate with this ratio in genusSaguinus andCallithrix, indicating that longer jaw in shape had relatively large M2. The reduction indices of two possible subspecies,S. oedipus geoffroyi andS. o. oedipus, were 36.1 and 47.3, respectively. This difference suggested that there was a difference in diet or function of jaw apparatus beyond subspecies level.     

Geographical variations in the cranium ofSaguinus geoffroyi

In terms of craniometry, we examinedHershkovitz's hypotheses that, inSaguinus geoffroyi, populations on the western shore of the Rio Atrato were closely related toS. leucopus, and that a morphocline could be traced from the easternS. geoffroyi population to the western one. We detected a morphological sequence from east to west (or east to west) but did not find any evidence supporting the former hypothesis.     

Evolutionary trends of the hairy-faceSaguinus in terms of the dental and cranial morphology

Shape variations in the dentition and the cranium were analyzed for sevenSaguinus forms of the hairy-face tamarin by applying the factor analysis method. The results obtained for the dental and cranial measurements were almost consistent with each other. The magnitude of the difference in shape factors between theS. nigricollis group and theS. midas group is appreciably larger than that between the former group and theS. mystax group. If the ancestral geographic centre of origin is postulated as being within the region which is inhabited by the livingS. nigricollis group, the morphological distances between any pairs of groups correlate well with the geographic distances between them. Concerning the dental and cranial morphologies, the physical changes in the three species group probably took place in two directions; that is, from theS. nigricollis group to theS. mystax group, and from theS. nigricollis group to theS. midas group. The forms belonging to each species group are more closely related to each other, with the exception ofS. imperator in theS. mystax group. The uniqueness ofS. imperator was clearly demonstrated by factor analysis and distance analysis. In theS. mystax group, although still hypothetical,S. imperator may have been related only through the basic ancestral stock toS. labiatus andS. mystax.     

Systematics of the Saguinus oedipus group of the bare-face tamarins: Evidence from facial morphology

The systematics of the Saguinus oedipus group within the bare-face tamarins remains open to question. Hershkovitz (Living New World Monkeys (Platyrrhini), Vol. 1. Chicago: University of Chicago Press, 1977) places the cotton-top and rufus-naped tamarins as subspecies of Saguinus oedipus (S. o. oedipus and S. o. geoffroyi, respectively). In contrast, several other authors have argued that these two taxa should be considered separate species (S. oedipus and S. geoffroyi). Phylogenetic relationships within the group are also disputed. Resolving these different interpretations has been difficult in part because no study of this group has included an objective measure of expected levels of specific vs. subspecific variation. We used facial measurements from 179 adult crania to address the systematics of this group and included a related species that is known to include multiple subspecies. Our sample included three taxa from the S. oedipus group of the bare-face tamarins (S. oedipus, S. geoffroyi, and S. leucopus) and six subspecies from the related hairy-face tamarin species S. fuscicollis. Comparisons to S. leucopus provided a relative measure of species-level differences. Analyses that included S. fuscicollis provided a measure of subspecific variation. There was no evidence of facial sexual dimorphism in any of these taxa. A variety of multivariate statistical analyses including discriminant function and cluster analysis suggest that S. oedipus and S. geoffroyi differ morphologically at a level consistent with species-level distinctions. The extent of differences between these taxa is large. The differences in their facial morphology was on the order of differences between S. oedipus or S. geoffroyi and S. leucopus rather than the extent of variation among S. fuscicollis subspecies. Furthermore, a comparison of collecting localities revealed that the variation we observed among S. oedipus and S. geoffroyi was not clinal but presented a large morphological discontinuity at the boundary between taxa. Our analyses also suggested that S. leucopus is more similar to S. oedipus than is either to S. geoffroyi. Finally, it may be that there are some distinct species within the S. fuscicollis group. However, this hypothesis, along with other phylogenetic relationships suggested by this study, will require more data and further study. © 1992 Wiley-Liss, Inc.     

Variations in dental measurements between Saguinus species and their systematic relationships.

Multivariate analysis is applied to dental measurements of Saguinus species to analyse their systematic relationships. The shape distance between Saguinus midas midas and S. midas niger is larger than that between S. nigricollis and S. fuscicollis, both of which are generally recognized as valid species. In dental form, S. bicolor is the closest relative of S. midas. S. inustus is not linked to S. leucopus. S. geoffroyi and S. leucopus, as S. inustus shows closer affinity with S. labiatus and S. mystax than with the former 3 species.     

Hand specialization, sympatry, and mixed-species associations in callitrichines

Hand morphology in callitrichines (i.e., tamarins, marmosets, and Goeldi's monkey) is correlated with positional and foraging behaviors. This study examines hand shape in callitrichines using an allometric approach. It addresses a series of questions relating hand anatomy, insect foraging behavior, and resource partitioning in callitrichines. The main questions are: 1. Do the hands of Leontopithecus differ in shape from all other callitrichine taxa allowing it to perform highly manipulative prey foraging behaviors? 2. Are the hands of Saguinus fuscicollis adapted to manipulative foraging, and are they functionally similar to Leontopithecus' hands? 3. Is hand morphology in S. fuscicollis more similar to the hand morphology of sympatric tamarin species with whom it does not form mixed species troops (S. nigricollis and S. tripartitus) than to those sympatric tamarin species with whom it does form mixed troops (S. mystax, S. labiatus, and S. imperator)? Measurements of hand length (HL), width (HW), and thickness (HT) were taken from 1350 museum specimens of callitrichines (Callithrix, Cebuella, Leontopithecus, Saguinus, and Callimico), squirrel monkeys (Saimiri), and owl monkeys (Aotus). The analysis indicates that hand shape covaries with foraging strategy. Specifically, the hands of Leontopithecus are adapted for manipulative foraging and are relatively longer and more slender than the hands of other callitrichines. A similar pattern is observed in the hands of S. fuscicollis, S. tripartitus and S. nigricollis. These latter species, however, differ significantly in shape from all other tamarin species. Large differences in hand morphology are observed among tamarin species that form mixed-species troops. These anatomical differences may permit resource partitioning and coexistence among these closely related taxa. Hand shape, expressed as log HLGM (logged hand length divided by the geometric mean of all measurements), is a good predictor of manipulative and non-manipulative prey foraging techniques employed by callitrichines.     

Numerical analysis of the taxonomical status ofCallithrix kuhli based on measurements of the postcanine dentition

The postcanine dentition ofCallithrix geoffroyi, Callithrix penicillata, andCallithrix kuhli was compared metrically to determine whetherC. kuhli is a hybrid population ofC. geoffroyi andC. penicillata or not. Many measurements showed significant differences (p<0.01 orp<0.05) among the three marmosets. The dental variability inC. kuhli was not greater than those inC. geoffroyi andC. penicillata. Based on canonical analysis, the three marmosets are discriminated, andC. kuhli did not occupy a middle position betweenC. geoffroyi andC. penicillata on the first two canonical axes. In the projection of the first two principal components,C. penicillata tended to be distinguished fromC. geoffroyi andC. kuhli, andC. kuhli does not exhibit intermediacy betweenC. geoffroyi andC. penicillata. The present statistical analysis failed to provide evidence thatC. kuhli constitutes a population hybridized fromC. geoffroyi andC. penicillata, although the three marmosets were discriminated from each other. This may provide support for the hypothesis thatC. kuhli is not a hybrid population ofC. geoffroyi andC. penicillata but a distinct species.     

Interspecific relationships ofCallithrix based on the dental characters

The dental structure of all species ofCallithrix, C. argentata, C. humeralifer, C. aurita, C. flaviceps, C. geoffroyi, C. penicillata, andC. jacchus is examined.Callithrix are divided intoC. jacchus group andC. argentata group, based on the analysis of dental characters.C. jacchus group consists ofC. jacchus, C. penicillata, C. geoffroyi, C. flaviceps, andC. aurita, whileC. argentata andC. humeralifer are assigned toC. argentata group. InC. jacchus group,C. aurita andC. flaviceps were differentiated from the original stock of their common ancestor, followed byC. geoffroyi, last byC. penicillata, and finallyC. jacchus. Based on the relationships among species ofCallithrix, it is possible to infer the relative age of the formation of the refuges which caused their speciation. First, the forests in southeastern Brazilian coast were split from Amazonia. In southeastern Brazilian coast, the Paulista center separated, followed by the Rio Doce center, the Bahia center, finally by the Pernambuco center.     

Craniometrical variations among eastern Brazilian marmosets and their systematic relationships

The craniometrical variations among marmosets on the eastern coast of Brazil or theCallithrix jacchus group (C. jacchus, C. penicillata, C. kuhli, C. geoffroyi, C. flaviceps, andC. aurita) were analyzed to test various hypotheses for the arrangement of the species and phylogenetic relationships ofC. kuhli andC. flaviceps. Q-mode correlation coefficients and principal component analysis were employed to extract important shape factors from the craniometrical data. On this basis, the shape distances among the eastern Brazilian marmosets were found to be larger than those between the marmosets which are recognized as distinct species. This evidence supports the hypothesis that the members of theC. jacchus group are distinct species.C. kuhli shows the strongest resemblance toC. geoffroyi within theC. jacchus group.C. flaviceps is the most similar toC. aurita in its cranial shape. These findings indicate thatC. kuhli is most closely related toC. geoffroyi, whileC. flaviceps is toC. aurita.     

Phylogenetic relationships of the callitrichinae (Platyrrhini,Primates) based on β2‐microglobulin DNA sequences

The phylogenetic relationships of callitrichine primates have been determined by DNA sequence analyses of exons 1, 2, and 3 of the β₂‐microglobulin gene. Parsimony, distance, and maximum likelihood analyses of ca. 900 base pairs of 21 taxa, representing all callitrichine genera, indicated that Saguinus was the most basal offshoot. Within Saguinus, S. fuscicollis appeared as the first divergent lineage followed by an unresolved trichotomy formed by S. mystax/S. imperator, S. midas/S. bicolor, and S. oedipus. A second callitrichine lineage was formed by Leontopithecus; each of the three species studied showed identical nucleotide sequences. Callimico appeared as the sister taxon of Callithrix/Cebuella. Genetic distances within this latter group were very small, although a stronger association between Cebuella and species of the Callithrix argentata group was observed. The inclusion of Cebuella in the genus Callithrix is suggested. These studies indicated that tamarins are more plesiomorphic than marmosets in agreement with the phyletic dwarfism hypothesis. Am. J. Primatol. 48:225–236, 1999. © 1999 Wiley‐Liss, Inc.     

A taxonomic study of KoreanSmilacina

Several taxonomic problems of KoreanSmilacina were examined by statistical methods, based on morphological data. Consequently,S. davurica described in Korean flora differs greatly from originalS. davurica, and closely related toS. bicolor morphologically. Therefore, the present authors treated this new taxon as a variety ofS. bicolor, S. bicolor var.flavovirens N. S. Lee et J. Y. Kim var. nov (“Yondusomdae” in Korean). The distribution in South Korea ofS. bicolor var.bicolor is known as only Mt. Chiri, but this species is collected in Mt. Dukyou, also. The bounds of morphological variations ofS. japonica var.japonica, the short plant size and no hairs on the stem, were revealed. The morphological characteristics ofS. japonica var.japonica andS. japonica var.mandshurica is obscure to distinguish. According to the present study,S. japonica var.mandshurica differs fromS. japonica var.japonica in plant size, size of adaxial leaf epidermal cell, ratio of style/ovary length and shape of stigma. The unrecorded taxon in Korean flora,S. robusta, was given a new Korean name as “Kunsomdae.” AlthoughS. japonica var.mandshurica is the variety ofS. japonica var.japonica, it is more closely related toS. robusta than toS. japonica var.japonica.     

Responses of Captive Single- and Mixed-Species Groups of Saguinus to Novel Nonthreatening Objects

The provision of novel objects allows one to probe for behavioural differences among species. This is particularly relevant when studying species that form mixed-species groups, as divergent responses may provide clues to the advantages that individuals gain from associating. We compared the responsiveness to novel objects in captive single- and mixed-species groups of saddleback (Saguinus fuscicollis) and red-bellied (Saguinus labiatus) tamarins to determine the influence of a congener. We tested groups with novel objects placed near the top, the middle, and on the floor of their enclosures and measured latency to approach and touch them. We tested predictions related to differences in lifestyle patterns under natural conditions. As we predicted, S.labiatus, which usually occur at a higher mean height in the forest than their congeners, responded to objects placed near the top of the enclosure significantly quicker in both single- and mixed-species groups. S. fuscicollis responded to objects placed on the floor quicker, and in mixed-species groups S. fuscicollis approached them before S. labiatus did. There were specific differences in median touch–approach time (T-A): Saguinus fuscicollis had a shorter T-A time than that of S. labiatus, which can be related to their manipulative foraging style. Reaction times decreased in mixed-species trials for both species, suggesting that the reaction of one species may effect the congener. Both species may benefit through association, though the dominance of Saguinus labiatus over S. fuscicollis may limit the advantages to S. fuscicollis. Over all our study supports the idea that cross-specific social facilitation is an important consequence of mixed-species groups of Saguinus.     

Primate censusing in northern Colombia: A comparison of two techniques

Five primate species were observed in an 83 hectare study site in northern Colombia. They wereAlouatta seniculus, Aotus trivirgatus, Ateles belzebuth hybridus, Cebus albifrons, andSaguinus leucopus. Average group size for the four diurnal species ranged from 5.3 individuals per sighting forCebus to 3.3 forAlouatta andAteles. BecauseCebus utilized regenerating forest, mature stands as well as cultivated sectors, they were able to use 30% more of the study site than the larger cebids. Monkey sightings along transects peaked at 0600–0800 and 1500–1800 and were lowest between 0900–1300 for the four diurnal cebids. The hourly rate of sighting the large cebids was 2–3 times greater for the point method than the transect method, but was less forCebus andSaguinus. However, consistently higher crude density estimates were obtained by the transect method than by the point method. As expected, there was less discrepancy between census methods for the large cebids which regularly utilized the upper canopy. The point method was barely 20% as effective as the transect method for estimating crude densities ofCebus andSaguinus. Factors influencing the effectiveness of the two census techniques as monkey detection and visibility, climatic conditions, and length of study are discussed. Recommendations for improving censusing effectiveness are listed.     

Protein variation,taxonomy and differentiation in five species of marmosets (genusCallithrix Erxleben, 1777)

The electrophoretic patterns of 15 protein systems codified for 20 genetic loci were investigated using horizontal electrophoresis. A total of 150 blood samples, from five species of the genusCallithrix were analyzed. Polymorphic variation was observed in 10 out 20 loci analyzed. The genotypic distributions are in Hardy-Weinberg equilibrium. The average heterozygosity (H) varied from 1% to 5%, similar to those observed for other Neotropical primates. The genetic distance coefficients revealed a phylogenetic separation of these species into two groups: (1) “argentata” (C. humeralifer andC. emiliae); (2) “jacchus” (C. jacchus, C. penicillata, andC. geoffroyi). This arrangement is according to the taxonomic arrangement proposed byHershkovitz (1977),de Vivo (1988), andMittermeier et al. (1988). The results in each group are compatible with the subspecies values recorded for the Platyrrhini. These values showed that:C. humeralifer andC. emiliae are subspecies ofC. argentata;C. jacchus, C. penicillata, andC. geoffroyi are subspecies ofC. jacchus. These results also suggest thatC. j. geoffroyi is the “jacchus” group taxon, most similar genetically to the “argentata” group.