Preliminary Report on the Distribution of <Emphasis Type="Italic">Callicebus oenanthe</Emphasis> on the Eastern Feet of the Andes

In 2007 we conducted a field study of almost 6 mo to determine the distribution of Callicebus oenanthe, formerly known as the Andean titi monkey. There previously has been no extensive study on the distribution and status by other fieldworkers. We visited a total of 96 localities within or around the presumed distribution of this rare primate species to determine the distribution of Callicebus oenanthe. We collected additional information on group size and threats to the species. Our expeditions revealed that the species is not endemic to the Alto Mayo Valley, as earlier authors suggested, but that its distribution extends into the Bajo Mayo and Huallaga Central. The study area is heavily deforested, and to date only one area was found where a viable population might live, although further research is needed to confirm this. The species lives in the southern part of its distribution in sympatry with another, undescribed species of Callicebus. We will continue the study to determine more precisely the distribution and conservation status of the Callicebus oenanthe, to determine if conservation measures are necessary for this species. This is the first activity of a long-term project for the conservation of Callicebus oenanthe initiated by La Vallée des Singes Primate park.     

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.     

Commitment to the care and management of chimpanzees: State-of-the-art developments in facility design,genetics, and environmental enrichment. Review of chimpanzee conservation and public health: Environments for the future,by Joe Erwin and John C. Landon,Editors. Diagnon/Bioqual,Inc., 1992, 171 pp., $40.00

The hypothesis of Kinzey and Gentry [Primate Ecology: Problem Oriented Field Studies. New York, John Wiley & Sons, 1979] that Callicebus torquatus may be specialized for living in vegetation on white sand was evaluated by reviewing all observations I made of this species, where the substrate had been noted, and including some collection sites of J. Hernández Camacho. There was no evidence for the white-sand hypothesis. Instead, Callicebus torquatus was found to prefer upland and flooded forests that are tall and well stratified, and growing on many soil types, including white sand. © 1994 Wiley-Liss, Inc.     

Food Choice in Masked Titi Monkeys (Callicebus personatus melanochir): Selectivity or Opportunism?

I investigated whether the food choice in masked titi monkeys (Callicebus personatus melanochir) is selective with respect to energy or phytochemical characteristics of the food resources or opportunistic in relation to food abundance. I collected data on food choice and availability of food resources for 1 year in a forest fragment of the Atlantic rain forest in Eastern Brazil and analyzed main food items of the masked titi monkeys—fleshy fruit parts, seeds, and young leaves—for protein, lipid, carbohydrates, acid detergent fiber, tannin, and total energy content. A rich season of high food availability is distinct from a lean season with low food availability. Effects of food chemicals on food selection are not apparent. The main factor in food choice in both seasons is the abundance of the food items. Thus, for Callicebus personatus melanochir, opportunistic foraging seems to be the optimal strategy.     

Species,subspecies, or color morphs? Reconsidering the taxonomy of <Emphasis Type="Italic">Callicebus</Emphasis> Thomas, 1903 in the Purus–Madeira interfluvium

There have been recent disagreements as to how many taxa of titi monkeys, genus Callicebus, occur in the region between the Purus and Madeira rivers in western Brazilian Amazonia. Three parapatric taxa were proposed for the area: Callicebus caligatus, Callicebus stephennashi, and Callicebus dubius, but the latter has recently been considered a synonym of C. caligatus, even though both form monophyletic groups and are morphologically distinct. We analyzed the geographic variation in the pelage of Callicebus occurring between the Madeira and Purus rivers and concluded that the phenotypes attributed to C. caligatus and C. dubius are not individual morphs, but rather well-marked and geographically restricted varieties. For this reason, we classify Callicebus caligatus as a polytypic species with two subspecies: Callicebus caligatus caligatus and Callicebus caligatus dubius. This classification is corroborated by molecular evidence as well. The morphological and distributional data indicate that Callicebus stephennashi is a hybrid form of C. c. caligatus and C. c. dubius, due to the presence of intermediate characters. Therefore, until more precise locality records are provided and further evidence is presented, we consider Callicebus stephennashi to be a homonym of the two parental forms.     

An ecological comparison of two sympatric primates:Saguinus fuscicollis andCallicebus moloch of Amazonian Peru

The ecologies of two sympatric primates,Saguinus fuscicollis andCallicebus moloch, were compared during a four-month field study in southeastern Peru in order to examine the mechanisms by which these primate frugivores minimize competition for food and space.Saguinus fuscicollis andCallicebus moloch were found to differ dramatically both in diet and in use of the shared habitat. Specifically, tamarins and titis showed very little overlap in their choices of food plants or animal foods and they used distinctive foraging styles, exploiting very different parts of the habitat for animal prey. Significant interspecific differences were found in the use of particular support structures and strata within the forest, and in the density of vegetation preferred. These results suggest that resource competition between saddle-backed tamarins and dusky titis is minimal, a fact that could account for the high frequency of free association between the two species and the benign nature of these interspecific contacts.     

Color Vision Variation and Foraging Behavior in Wild Neotropical Titi Monkeys (<Emphasis Type="Italic">Callicebus brunneus</Emphasis>): Possible Mediating Roles for Spatial Memory and Reproductive Status

The selective advantages to primates of trichromatic color vision, allowing discrimination among the colors green, yellow, orange, and red, remain poorly understood. We test the hypothesis that, for primates, an advantage of trichromacy over dichromacy, in which such colors are apt to be confused, lies in the detection of yellow, orange, or red (YOR) food patches at a distance, while controlling for the potentially confounding influences of reproductive status and memory of food patch locations. We employ socially monogamous titi monkeys (Callicebus brunneus) which, like most platyrrhine primates, have polymorphic color vision resulting in populations containing both dichromatic and trichromatic individuals. Wild Callicebus brunneus spent most foraging time in YOR food patches, the locations of most of which were likely to have been memorable for the subjects. Overall, both dichromatic and trichromatic females had significantly higher encounter rates than their dichromatic male pair mates for low-yield ephemeral YOR food patches whose locations were less likely to have been remembered. We detected no difference in the encounter rates of dichromatic and trichromatic females for such patches. However, the data suggest that such a difference may be detectable with a larger sample of groups of Callicebus brunneus, a larger sample of foraging observations per group, or both. We propose that a trichromatic advantage for foraging primates may be realized only when individuals’ energy requirements warrant searching for nonmemorable YOR food patches, a context for selection considerably more limited than is often assumed in explanations of the evolution of primate color vision.     

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.     

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.     

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.     

Trypanoxyuris croizati n.sp. andT. callicebi Hugot & Vaucher, 1985 (Nematoda: Oxyuridae), two vicariant forms parasitic inCallicebus spp. (Primatia,Cebidae)

Trypanoxyuris croizati n. sp., a parasite ofCallicebus torquatus from Venezuela, is described. The following characters differentiate the new species from the nearest species,Trypanoxyuris callicebi Hugot & Vaucher, 1985 fromCallicebus moloch in Paraguay: inT. callicebi, (i) the hexagonal feature of the cephalic outline is less marked; (ii) crests forming the lateral alae are more developed; (iii) the body is less than half as wide; (iv) the oesophagus is much shorter and the oesophageal bulb less voluminous; (v) the excretory pore and the vulva are closer to the anterior extremity; (vi) the tail is much longer; and (vii) the eggs are more voluminous and their major axis is more elongate.T. callicebi andT. croizati n. sp. are considered to be vicariant forms, stemming from the same species when two populations and their respective hosts were isolated by a geographical barrier, the Amazon. The distribution of these two parasites, which closely matches the zoogeography of hosts, reinforces the hypothesis of Cameron (1929) who postulated a strict co-evolution of primates and their oxyurid parasites.

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Résumé Trypanoxyuris croizati n. sp., parasite d'unCallicebus torquatus du Venezuela, est décrite. La nouvelle espèce diffère de l'espèce la plus proche,T. callicebi Hugot & Vaucher, 1985, décrite chez unCallicebus moloch du Paraguay, pour les caractères suivants: chezT. callicebi, (i) la forme hexagonale du contours céphalique est moins marquée; (ii) les crêtes constituant les ailes latérales sont plus développées; (iii) la largeur du corps est inférieure presque de moitié, (iv) l'oesophage est relativement beaucoup plus court et le bulbe oesophagien moins volumineux; (v) le pore excréteur et la vulve sont plus rapprochés de l'apex; (vi) la queue est beaucoup plus longue; (vii) les oeufs sont plus volumineux et leur grand axe est plus allongé.T. callicebi etT. croizati n. sp. sont interprétées comme des formes vicariantes, issues d'une même espèce parasites dont deux populations, et leurs hôtes respectifs, se sont trouvés isolés par un obstacle géographique, le cours de l'Amazone. La répartition de ces parasites, qui souligne de façon étroite la zoogéographie de hôtes, renforce l'hypothèse de Cameron (1929), qui supposait l'existence d'un phénomène d'étroite co-évolution entre les Primates et leurs oxyures.

     

Evaluating the genetic status of a closed colony of titi monkeys (Callicebus cupreus) using multigenerational pedigrees

Pedigree metrics are essential for investigating colony genetic structure. The genetic structure of a closed Callicebus cupreus colony was examined using multigenerational pedigrees. Inbreeding was low, but genetic drift caused the loss of founder genome representation. Pedigrees can be used to detect founder representation and prevent bottlenecks and allele loss.     

Intergroup loud calls,range size,and spacing in Callicebus torquatus

Observations are reported on the response of a free-ranging group of Callicebus torquatus to recordings of loud intergroup calls. When the recording consisted of the call of a solo adult male, the group fled from the recording. When the recording consisted of the adult male and female duetting together, the group remained in place and called back to the recording. These results contrast with previously described vocal and spatial responses of C. moloch and suggest that range size influences the mechanisms that regulate between-group spacing. The consequence of intergroup loud calls in C. moloch is to define and reinforce the location of boundaries, whereas in C. torquatus, homologous calls maintain spacing between groups.     

Divergence between biochemical and cytogenetic differences in three species of the Callicebus moloch group

Specimens from three species of the Callicebus moloch group—C. Moloch (N = 80), C. brunneus (N = 166), and C. cupreus (N = 23)—were studied. Twenty genetic loci were investigated through electrophoresis, genetic distances were estimated, and the results compared with the available cytogenetic data. Low values of genetic distance were encountered, contrasting with relatively large chromosome differences. We propose that recent karyotypic rearrangements, rather than other Pleistocene events, were the major evolutionary mechanisms determining speciation in these three taxa. © 1993 Wiley-Liss, Inc.     

Species differences in adrenocortical activity of new world primates: Response to dexamethasone suppression

The effect of dexamethasone-induced alteration of adrenocortical activity was assessed in two species of New World primates: Saimiri sciureus and Callicebus moloch. Basal and stress levels of corticosteroids were determined following treatment with three doses of dexamethasone (0, 50, or 500 μg/kg). Saimiri showed substantially higher basal levels of corticosteroids than did Callicebus and a greater incremental corticosteroid response to physical restraint. Dexamethasone was found to reduce basal corticosteroids in both species, although this effect was greater for Callicebus than for Saimiri Moreover, the adrenocortical response to physical restraint was reduced by dexamethasone treatment in Callicebus but not in Saimiri. The pattern of results suggests that the species differ in the mechanisms mediating adrenocortical activity.     

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.     

Sequences from the 5′ flanking region of the ϵ‐globin gene support the relationship of Callicebus with the pitheciins

The purpose of this study was to determine nucleotide sequences from the 5′ flanking region of the ϵ‐globin gene of selected platyrrhine primates and to analyze the data for phylogenetic information and estimated times of divergence. We report new sequence data for two species of New World monkeys, Callicebus torquatus and Pithecia irrorata. We analyzed these data in conjunction with homologous sequences from other primate species. The data support the hypothesis that the titi monkeys (Callicebus) and seed predators (Tribe Pitheciini) form a clade (Subfamily Pitheciinae), and also provide limited support for that subfamily being allied with the atelines. We also present estimated dates of divergence for the Callicebus and pitheciin lineages. Am. J. Primatol. 48:69–75, 1999. © 1999 Wiley‐Liss, Inc.     

Phylogeny and Evolution of Selected Primates as Determined by Sequences of the ε-Globin Locus and 5′ Flanking Regions

We studied phylogenetic relationships of 39 primate species using sequences of the -globin gene. For 13 species, we also included flanking sequences 5 of this locus. Parsimony analyses support the association of tarsiers with the anthropoids. Our analysis of New World monkeys supports the model in which the callitrichines form a clade with Aotus, Cebus, and Saimiri, with Cebus and Saimiri being sister taxa. However, analysis of the 5 flanking sequences did not support grouping the atelines with Callicebus and the pitheciins. Our data support the classification of platyrrhines into three families, Cebidae (consisting of Cebus, Saimiri, Aotus, and the callitrichines; Atelidae—the atelines; and Pitheciidae—Callicebus and the pithiciins. The strepsirhines form well-defined lemuroid and lorisoid clades, with the cheirogaleids (dwarf and mouse lemurs) and Daubentonia (aye-aye) in the lemuroids, and the aye-aye being the most anciently derived. These results support the hypothesis that nonhuman primates of Madagascar descended from a single lineage. Local molecular clock calculations indicate that the divergence of lemuroid and lorisoid lineages, and the earliest diversification of lemuroids, occurred during the Eocene. The divergence of major lorisoid lineages was probably considerably more recent, possibly near the Miocene–Oligocene boundary. Within hominoids some estimated dates differ somewhat from those found with more extensive noncoding sequences in the -globin cluster.     

Pathological and parasitological findings in a wild red titi monkey, <Emphasis Type="Italic">Callicebus cupreus</Emphasis> (Pitheciidae,Platyrrhini)

An adult female red titi monkey (Callicebus cupreus) was found in a moribund state below a sleeping site at the Estación Biológica Quebrada Blanco in Peruvian Amazonia. Before death, the animal showed frequent convulsions. Post-mortem examination revealed the presence of Prosthenorchis elegans (Acanthocephala) in the small intestine. Major pathological findings concerned the digestive tract and the liver. Adult P. elegans provoked multifocal subacute to chronic enteritis with formation of ulcers in the small and large intestine. The liver revealed a severe chronic-active granulomatous hepatitis. While the cause of death could not be unambiguously identified, the infestation with P. elegans is likely to have played a key role in the pathogenesis of the chronic ulcerative enteritis and subsequent hepatitis; it possibly had a severe and long-term impact on the host’s resource utilisation and defence against intruding pathogens and toxins of the digestive tract. The death of the animal is attributed to the chronic inflammatory processes in the digestive tract.     

Observed case of maternal infanticide in a wild group of black-fronted titi monkeys (<Emphasis Type="Italic">Callicebus nigrifrons</Emphasis>)

A maternal infanticide was observed in a group of unprovisioned wild black-fronted titi monkeys (Callicebus nigrifrons). An approximately 3-day-old male infant was killed by his mother. A post-mortem revealed the infant to be clinically healthy. We considered various hypotheses to explain why this behavior occurred (e.g., reproductive advantage, stress, nutritional, infant viability and population density). It is noteworthy that the mother and not the father killed the infant, since in this species the father provides considerable infant care from a few hours after birth.