The lowest diploid number (2n = 16) yet found in any primate: Callicebus lugens (Humboldt, 1811)

Morphologic, molecular and karyologic analyses of Callicebus lugens (Humboldt, 1811) of known geographic origin supported the proposition that this is a valid species. Morphologic and morphometric analyses showed evident differences between C. lugens and two other related taxa of the same group (Callicebus purinus and Callicebus torquatus). Cytochrome b DNA analyses (maximum parsimony, neighbour joining and maximum likelihood) were congruent in showing a strong association between C. lugens and Callicebus sp. of the torquatus group in one branch and a sister branch further divided into two clades: one with species of the personatus group and another, with species of the moloch group. Karyotypic analysis showed that C. lugens has the lowest diploid chromosome number of the primate order (2n = 16). Comparisons with other congeneric species clearly supported the proposition that C. lugens is karyotypically similar to others of the torquatus group.     

A new karyotype of an endangered primate species (Callicebus personatus) from the Brazilian Atlantic forests

The genus Callicebus has 28 species arranged in five groups: donacophilus, torquatus, moloch, cupreus and personatus. The personatus group occurs in the Brazilian Atlantic forests where it is isolated from the other Callicebus groups. The present paper is the first report on the karyotype of Callicebuspersonatus. We compared the karyotypes of C. personatus and C. nigrifrons utilizing the following classic banding techniques: G-, C-, NOR banding, G/C- and G/NOR sequential banding. The karyotype of C. personatus has 2n=44, while C. nigrifrons presented 2n=42. Both the species diverge in the diploid number in consequence of a rearrangement type centric fusion/fission. Our results support personatus as a valid group and the specific status for C. personatus and C. nigrifrons.     

Phylogeographic analyses of Callicebus lugens (Platyrrhini, Primates)

A phylogeographic study of Callicebus lugens was carried out based on cytochrome b DNA sequence data. Here, we report, for the first time, the distribution of C. lugens south of the Rio Negro, in Barcelos municipality (Amazonas State, Brazil), indicating that this river is not the southern boundary of the distribution of this species as previously proposed. Specimens from the north and south banks showed the same diploid number (2n = 16), while phylogenetic reconstructions based on maximum parsimony, distance, and maximum likelihood analyses grouped all specimens in a strongly supported clade comprising 2 separate lineages, in coincidence with their geographic distribution along riverbanks. Median-joining analysis showed a similar separation, with 22 transitions between the 2 groups, whereas time of divergence estimates indicated that the splitting of the C. lugens lineages occurred some 2.2 million years before present. Conservation strategies should take into consideration that this species might be sympatric with Callicebus torquatus at the south bank of Rio Negro.     

A new karyotype in Callicebus torquatus (Cebidae, Primates)

We describe a new karyotype of Callicebus torquatus using conventional staining, G-banding with Wright Stain, CBG, Ag-NOR staining and fluorescence in situ hybridization (FISH) with human telomere probes and comparative analysis with the previously reported karyotype of C. torquatus torquatus (2n = 20). We studied a female specimen maintained in captivity at the Centro Nacional de Primatas (Para, Brazil). This titi monkey presented 2n = 22, with four large biarmed and six acrocentric autosome pairs; the X chromosome is a medium submetacentric. C-bands were revealed at the centromeric region of all acrocentrics and X chromosome; punctual C-bands also are visualized at the centromeric region in the large biarmed pairs. The NOR site was located at the long arm of pair 4, at the position of a conspicuous secondary constriction. Hybridization signals were detected exclusively at the terminal region of all chromosomes. The karyotype described here has one acrocentric pair more than that found in the literature and also differs by amount and distribution of constitutive heterochromatin. Our data support the notion that the torquatus group may be composed of distinct species, each with its own karyotype.     

Titi monkeys (Callicebus spp., Atelidae: Platyrrhini) in the Brazilian state of Rondônia

Five species of titi monkey (Callicebus brunneus, Callicebus caligatus Callicebus cinerascens, Callicebus donacophilus, andCallicebus moloch) were recorded in surveys of primate populations at 26 sites throughout the Brazilian state of Rondônia. The distribution of the two species,C. cinerascens andC. donacophilus (recorded in the state for the first time), appeared to be related to that of non-forest ecosystems, the former in thecerrado woodlands, and the latter in gallery forests of the Guaporé grasslands. The results of the surveys also indicate thatC. brunneus has a more restricted distribution in southern Rondônia than was previously thought, whereasC. moloch is more widespread. However, the ecological factors that determine species distribution in the south of the state remain unclear on the basis of the available data. All species were observed in small social groups of no more than five individuals, which are typical of the genus, generally in the middle and lower forest strate.     

Genomic mapping of human chromosome paints on the threatened masked Titi monkey (Callicebus personatus)

Callicebus is a complex genus of neotropical primates thought to include 29 or more species. Currently, the genus is divided into 5 species groups: donacophilus, cupreus, moloch, torquatus and personatus. However, the phylogenetic relationships among the species are still poorly understood. This genus is karyotypically diverse and shows extensive variation in diploid number (2n = 16 to 50). To foster a better understanding of the chromosomal diversities and phylogenetic relationships among the species of Callicebus, we performed a chromosome-painting analysis on the Callicebus personatus genome using human probes, and compared the resulting hybridization map to those of previously mapped titi species. We detected 38 hybridization signals per haploid autosomal set of C. personatus. Few ancestral syntenies were conserved without rearrangement, but 4 human associations (HSA20/13, 3c/8b, 1b/1c and 21/3a/15a/14) were demonstrated to be apomorphic traits for C. persona tus. G-banding suggested that these associations are shared with C. nigrifrons and C. coimbrai (personatus group), while C. personatus is linked with C. pallescens (donacophilus group) by 2 synapomorphies: HSA10b/11 (submetacentric) and an inversion of HSA1a.     

Dermatoglyphic patterns and pattern intensities of Callicebus (primates: Cebidae): description and comparison of three species

The palmar and plantar dermatoglyphic pattern types are described for three species of Callicebus (18 Callicebus moloch, 18 Callicebus torquatus and 7 Callicebus personatus). Mean pattern intensities (API) were calculated for each of seven areas of the palm and nine areas of the sole, and a summed mean total pattern intensity (TPI) for each volar surface. Nonparametric statistical testing showed no significant bilateral asymmetry or sexual dimorphism in pattern intensities. Pattern profiles describing the relative relationships of API values across the left palm and sole are presented. The profiles typical of the genus closely resemble those of Aotus and Saimiri. Significant interspecific differences, particularly in the plantar API values, were detected. The results are discussed with reference to the present taxonomic classification of the species of Callicebus and their postulated evolutionary history.     

Comparative locomotion of six sympatric primates in Ecuador

Primates exhibit a great variety of arboreal locomotor modes associated with their size and postcranial morphology. The study of sympatric primates is interesting in that it may reveal how primates of different sizes and anatomies move and select for forest structure. This study reports on preliminary data on the locomotion of six non-ateline platyrrhines found in the Yasuni National Park, Napo Province, Ecuador. Pygmy marmosets are confined to the understory using scansorial locomotion and quadrupedalism, preferring large vertical supports. Golden-mantled tamarins, common squirrel monkeys and dusky titis also range in the understory, moving by quadrupedal walk and leap, mainly on small horizontal supports. Monk sakis are found in the main canopy and use quadrupedal walk and less leap on medium-sized horizontal supports. Whitefronted capuchins use the understory and the main canopy equally often, walking quadrupedally and leaping on small and medium-sized oblique supports. In general, smaller species occupy lower strata while larger species tend to spend more time in the upper strata. Small tegulae-bearing monkeys showed the highest proportions of large vertical support use. For all species, leaping was the main gap-crossing mode, though decreasing in proportion with a higher use of the upper forest layers.     

Evidence for insectivory in two primate species (Callicebus torquatus lugens and Lagothrix lagothricha lagothricha) from northwestern Amazonia

Insects were recovered and identified from stomach contents of two Callicebus torquatus lugens and one Lagothrix lagothricha lagothricha collected in a remote area of northwestern Amazonia. Both C. torquatus lugens showed little insect matter in stomach contents. Conversely, a minimum of 133 individual insects were recovered from stomach contents of the L. lagothricha lagothricha. These included various larger, rapid forms (Cicadellidae) unlikely to have been inadvertently consumed while the animal was eating fruit.     

Geographic distribution and possible taxonomic distinction of Callicebus torquatus populations (Pitheciidae: Primates) in Peruvian Amazonia

Population densities of yellow-handed titi monkey (Callicebus torquatus) were estimated using transect census methods. Densities were 2.8 individuals/km(2 )in the upper Rio Itaya basin and 2.5 individuals/km(2) in the lower Rio Algodón basin. Group size varied from two to five individuals, with an average of 2.9 individuals per group at the Rio Itaya. Groups were generally composed of two adults, probably the reproductive pair, with progeny from one to three previous birth seasons. Although the Rio Itaya population is phenotypically identical to populations from the rivers Nanay and Tigre, it differs from population on the rivers Napo and Putumayo. This suggests the existence of two disjunct populations of C. torquatus in Peruvian Amazonia whose taxonomic status warrants further examination.     

Locomotor behavior of Lagothrix lagothricha and Ateles belzebuth in Yasuní National Park, Ecuador: general patterns and nonsuspensory modes.

Field study of the locomotor behavior of sympatric woolly monkeys (Lagothrix lagothricha) and spider monkeys (Ateles belzebuth) in undisturbed rainforest of northern Ecuador revealed similar patterns in use of plant forms (categorized tree and liana structure), and substantial differences in the frequencies of use of different grouped modes (aggregates of kinematically similar specific modes). Lagothrix progressed more than Ateles by leaping/dropping and quadrupedal walking/running, whereas Ateles exhibited more suspensory locomotion. Grouped modes are associated with different plant forms in similar ways in the two species. In contrast, the species differed in use of tree zone (trunk/bole, major branches, intermediate branches, and terminal branches), with Lagothrix using intermediate branches and Ateles terminal branches more. Correlated with this difference was greater use by Lagothrix of quadrupedal movement, especially on intermediate branches, and greater use of suspensory modes by Ateles, especially in the terminal zone. Further research is needed to determine how these patterns are facilitated and constrained by morphological mechanisms. Analysis of specific locomotor modes within groups shows several interspecific differences in relative frequencies.     

Insect prey foraging strategies in Callicebus oenanthe in northern Peru

Titi monkeys (genus Callicebus) are small-bodied platyrrhines that supplement their predominantly frugivorous diet with variable amounts of leaves, seeds, and/or arthropod prey. Notable interspecific variation in the amount of insect prey in the diet has been observed in Callicebus, ranging from 0% to 20%. In this study, I investigate the degree and type of prey foraging in a little-known species, Callicebus oenanthe inhabiting a fragmented, secondary forest on the foothills of the Andes in northern Peru. I present data on prey type, prey search and capture techniques, substrate/vegetation use, foraging height, prey capture efficiency, and seasonal variation of insect prey foraging in one group of C. oenanthe observed from January to August 2005. Insect prey accounted for 22% of the diet, the highest amount reported for any Callicebus species to date, and insects from at least six different orders were included. C. oenanthe was mainly an investigative forager of hidden prey, manipulating easy-to-open substrates such as rolled up leaves, and hunted ant swarms and larger insects opportunistically. Insect foraging was predominant during the dry season (26%) and decreased during the wet season (13%). The study group foraged mostly in the understory (2-6 m) within vine-laden shrubs and trees, which may conform to an anti-predator strategy of crypticity. Overall the group had an 83% insect capture success rate. These data suggest that insect prey is an important part of the diet of C. oenanthe and may be especially notable during periods of resource scarcity. This study adds to the knowledge concerning insect prey foraging in Callicebus, which can have an important role in defining ecological strategies in the selection of secondary protein food resources within a given ecosystem.     

Positional behavior ofCebuella pygmaea in Yasuni National Park, Ecuador

In terms of positional behavior, the small-bodied callitrichids are distinguished from other anthropoids by their ability to leap between and to cling to large vertical supports, feeding occasionally or frequently on sap and bark insects. In this paper, I studied the positional behavior of a group of pygmy marmosets in a hilly wet tropical forest in Yasuni National Park, Ecuador. During traveling, the animals used quadrupedal walk/bound and leaping mostly on small horizontal supports. During foraging, quadrupedal walk/bound and clambering dominated. The main foraging postures were stand and cantilever, occurring mainly on small horizontal lianas. During feeding, scansorial locomotion was used very frequently. Claw clinging was the dominant feeding posture. Furthermore, large vertical lianas and tree boles were the most frequent feeding supports. These observations would suggest that scansorial locomotion, vertical clinging, and vertical leaping are most likelynot part of the same form function complex. Vertical leaps appear to be associated with moving in the lower parts of the forest. On the other hand, scansorial locomotion and vertical clinging appear to be related to feeding on the sap of tree boles and large lianas in the lower parts of the forest.     

Habitat use and support preference of two free-ranging saltatory lemurs (Lepilemur edwardsi and Avahi occidentalis)

Lepilemur edwardsi and Avahi occidentalis are two species of nocturnal, folivorous 'vertical clingers and leapers' (VCL). They have a similar body mass and share the same morphological adaptation for leaping. In a field study under sympatric conditions at Ampijoroa, Madagascar, comparison of support use with support availability using Jacobs' D preference values (Jacobs, 1974) showed that both species actively chose or avoided branches with certain qualities. However, while both species showed a preference for small oblique and horizontal branches, they selected them at different heights in the forest and with varying degrees of preference and avoidance for the other available supports. Despite their traditional locomotor assignation, both species showed a surprisingly strong preference for horizontal supports. These striking variations in detail of support preference may aid the maintenance of species segregation and niche difference.     

Forest use and activity patterns of Callimico goeldii in comparison to two sympatric tamarins, Saguinus fuscicollis and Saguinus labiatus

Callimico goeldii, Saguinus fuscicollis, and S. labiatus are sympatric in northern Bolivia and differ from each other in patterns of spatial and structural use of their environment. C. goeldii has a home range five times larger than that of mixed-species troops of S. fuscicollis and S. labiatus. The larger overlapping home range of C. goeldii allows it to move among Saguinus troops, giving it access to a wide range of different microhabitats. All three species use the most common microhabitat in the area, primary forest with dense understory, more than any other microhabitat type. C. goeldii habitat use varies by season, with bamboo and Heliconia microhabitats used more during the dry season. Each species shows preferences for different height classes: C. goeldii is found almost exclusively in the understory, S. fuscicollis uses the understory and middle canopy, and S. labiatus is found mostly in the middle canopy. These height class preferences are reflected in each species' locomotor styles, with C. goeldii showing the highest rates of vertical clinging and leaping, and S. labiatus showing the highest rates of branch-to-branch leaping and quadrupedal movement. The results suggest that C. goeldii may be restricted to forests with dense understory and a mosaic of other microhabitats. Furthermore, C. goeldii does not appear to use its tegulae for large branch foraging, but rather for vertical clinging and leaping between small vertical supports.     

Censusing primates by transect in a forest of known primate density

A series of four transect or strip censuses of primates was carried out in a forest in eastern Colombia where the absolute density of the three diurnal species had been previously calculated during long-term studies. The diurnal species were Alouatta seniculus, Callicebus torquatus,and Cebus apella.Techniques were identical, except for a few variables tested for their effect on the experimental results;these included three different types of detection distances. Variable results were obtained for the two species having the smallest home ranges (A. seniculusand C. torquatus)with the most consistently accurate densities being calculated using the drop in the frequency distribution of sighting distances as a measure of the detection distance. Grossly inflated results were obtained for almost all calculations of C. apelladensity. The stimulus leading to the detection of particular primate groups was usually their vocalizations. Counts of recognized group members were inaccurate and short of the actual number of individuals in each group. Problems of censusing primates are discussed and some recommendations are made with respect to the use of the transect census method.     

Extension of the Geographical Range of White-browed Titi Monkeys (<Emphasis Type="BoldItalic">Callicebus discolor</Emphasis>) and Evidence for Sympatry with San Martin Titi Monkeys (<Emphasis Type="BoldItalic">Callicebus oenanthe</Emphasis>)

White-browed titi monkeys (Callicebus discolor) have one of the largest distribution ranges of all titi monkey species, occurring from central Peru to southern Colombia. During a long-term study on the distribution of titi monkeys and other primates in Peru, we conducted extensive surveys in the San Martin Department of northeastern Peru. We encountered Callicebus discolor at the left bank of the Huallaga River, where the species most probably lives in sympatry with endemic San Martin titi monkeys (Callicebus oenanthe). Our study reveals an important extension of its formerly known distribution range. Massive deforestation activities in the region make studies on the habitat preferences of both species difficult, as most titi monkeys are confined to the remaining small remnants of the original forest. Urgent conservation measures are necessary to preserve the last lowland forests of San Martin.     

Prey foraging of red titi monkeys, Callicebus cupreus, in comparison to sympatric tamarins, Saguinus mystax and Saguinus fuscicollis

We compared the prey capture strategies of red titi monkeys, Callicebus cupreus, with those of sympatric mustached, Saguinus mystax, and saddleback tamarins, Saguinus fuscicollis, to examine whether animal prey is important in niche differentiation between these Neotropical primates. We collected data on strata and substrate use during foraging, on prey searching and capturing, and on prey type of two C. cupreus groups and one group each of S. mystax and S. fuscicollis during a 5-month field study in northeastern Peruvian Amazonia. Our results showed that C. cupreus differed both from S. mystax and S. fuscicollis in prey capture strategies: (1) C. cupreus used lower forest strata for prey search and capture than S. mystax and higher forest strata than S. fuscicollis. (2) C. cupreus captured prey on a higher variety of substrates than S. mystax and more often on open microhabitats compared to S. fuscicollis. (3) C. cupreus captured prey more often directly than S. mystax and rarely by manual search, in contrast to S. fuscicollis. (4) C. cupreus fed exclusively on arthropods and focused on Hymenoptera, in contrast to both tamarin species that focused on Orthoptera and included vertebrates in their diet. These findings indicate that animal prey plays a role in niche differentiation between C. cupreus and S. fuscicollis/S. mystax and might facilitate the coexistence of these three sympatric species.     

Canine teeth of the monkey,Callicebus moloch: Lack of sexual dimorphism

Unlike other primates, the South American titi monkey,Callicebus moloch, does not exhibit sex-differences in the size or shape of the canine teeth, or in the extent of loss or fracture from excessive use. Males and females have similar canines as well in each of six subspecies ofC. moloch. The lack of dimorphism is related to the low level of aggression in this species.     

Diet of a Group of Callicebus torquatus lugens (Humboldt, 1812) During the Annual Resource Bottleneck in Amazonian Colombia

A group of Callicebus torquatus lugens using a territory of 22.25 ha in eastern Colombia showed a varied diet throughout the annual period of lowest fruit availability. This is a time when the females are usually pregnant. During a 6-month period the study group's diet consisted of 59.4% fruits, 26.9% immature seeds, 6.4% leaves, 3.9% flowers, and 3.4% insects and spiders. At the fruit bottleneck, consumption of seeds and flowers increased, while consumption of leaves and insects showed no particular trend. They ate 62 species of plants: 45 for flesh, 6 for seeds, 2 for flowers, and 13 for foliage. The most important families in terms of species chosen are Moraceae (8 species, or 11 species if Cecropiaceae is included), Myristicaceae (7), Arecaceae (4), Chrysobalanaceae (4), and Euphorbiaceae. The most important families in terms of feeding time are Myristicaceae (25%), Euphorbiaceae (15%), Moraceae (14%), and Arecaceae (9%). Of 440 marked feeding trees in the territory of the group, 41.1% are represented by Sandwithia heterocalyx (Euphorbiaceae). This species is the most important food in the diet and has the highest density of all food trees in the home range. It followed by Heterostemon conjugates (Caesalpiniaceae) (10%), Iryanthera ulei (Myristicaceae) (6.1%), Anaxagorea brachycarpa (Annonaceae) (5.9%), and Iryanthera crassifolia (Myristicaceae) (3.4%). The remaining 33.5% of the marked trees are represented by the other 57 species. In terms of time spent feeding, the important trees in the diet include Sandwithia heterocalyx (13.9%), Virola melinonii (10%), Iryanthera ulei (8.35%), Oenocarpus bataua (7.06%), and Heterostemon conjugates (6.53%). We suggest that Callicebus torquatus should be described as a frugivore–granivore; they share with the Pitheciin an immature seed-eating adaptation.