Callicebus Research Articles

Phylogenetic relationships in the genus Cheracebus (Callicebinae, Pitheciidae).

Cheracebus is a new genus of New World primate of the family Pitheciidae, subfamily Callicebinae. Until recently, Cheracebus was classified as the torquatus species group of the genus Callicebus. The genus Cheracebus has six species: C. lucifer, C. lugens, C. regulus, C. medemi, C. torquatus, and C. purinus, which are all endemic to the Amazon biome. Before the present study, there had been no conclusive interpretation of the phylogenetic relationships among most of the Cheracebus species. The present study tests the monophyly of the genus and investigates the relationships among the different Cheracebus species, based on DNA sequencing of 16 mitochondrial and nuclear markers. The phylogenetic analyses were based on Maximum Likelihood, Bayesian Inference, and multispecies coalescent approaches. The divergence times and genetic distances between the Cheracebus taxa were also estimated. The analyses confirmed the monophyly of the genus and a well-supported topology, with the following arrangement: ((C. torquatus, C. lugens), (C. lucifer (C. purinus, C. regulus))). A well-differentiated clade was also identified within part of the geographic range of C. lugens, which warrants further investigation to confirm its taxonomic status.

Hand-rearing protocol and comparison of growth rates in parent reared versus hand reared offspring: a case study in Callicebus cupreus

The European Endangered Species Programme (EEP) for coppery titi monkeys (Callicebus cupreus) has a total population of 90 individuals within zoos that suffer from low reproduction rates and high neonatal mortality. Bristol Zoo Gardens (BZG) housed a breeding female from 2012 who first showed signs of pregnancy in 2017. During parturition, the female died from shock secondary to uterine prolapse. In order to ensure the survival of the infant it was hand-reared. This infant offered the opportunity to trial a hand-rearing protocol for Callicebus. The aim of this publication is to report the first detailed hand rearing protocol for the species and to compare the growth rates of two hand-reared infants against and seven parent-reared titi monkeys using information on growth rates gathered using ZIMS. Day had a significant effect on the weight of both hand-reared and parent-reared titi monkeys (F(1,57)=919.3, p<0.001, np2 =0.942). Parent-reared titi monkeys had significantly higher growth rates (457.9±9.3) compared to the hand-reared (390.7±11.1) titi monkeys (F(1,57)=19.804, p<0.001, np2 =0.258). Despite the differences in growth rates between the hand-reared and mother-reared infants the rearing protocol used was considered successful due to the infant being the first hand reared coppery titi monkey to survive to adulthood without any nutritional deficiencies. Further research is needed to develop this protocol to include more natural feeding and socialisation procedures to improve hand reared coppery titi monkey growth and development in captivity and other Callicebus species in the future.

Phylogeny, molecular dating and zoogeographic history of the titi monkeys (Callicebus, Pitheciidae) of eastern Brazil

The titi monkeys belong to a genus of New World primates endemic to South America, which were recently reclassified in three genera (Cheracebus, Plecturocebus and Callicebus). The genus Callicebus, which currently includes five species, is endemic to eastern Brazil, occurring in the Caatinga, Savanna, and Atlantic Forest biomes. In the present study, we investigated the validity of these species and inferred their phylogenetic relationships, divergence times, and biogeographic patterns based on the molecular analysis of a concatenated sequence of 11 mitochondrial and nuclear DNA markers, derived from 13 specimens. We ran Maximum Likelihood (ML) and Bayesian Inference (BI) analyses, and estimated genetic distances, divergence times. Ancestral areas were estimated on BioGeoBears. Our results suggest that at about twelve million years ago, the ancestor of all titi monkeys inhabited a wide area that extended from the Amazon forest to the South of the Atlantic forest. A first vicariant event originated Cheracebus in the West of the Amazon and the ancestor of Callicebus and Plectorocebus which, later were separated by a second one. The diversification of Callicebus occurred during the Plio-Pleistocene (beginning at 5 Ma) probably influenced by climatic fluctuations and geological events. Therefore, the results of the present work confirmed the existence of five species that currently inhabit forested areas under increasing threat from human activities. Thus, a reliable diagnosis of the taxonomic status of species living in endangered environments is extremely important for the development of conservation measures.

Species, subspecies, or color morphs? Reconsidering the taxonomy of Callicebus 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.

Phylogenetic relationships within the Callicebus cupreus species group (Pitheciidae: Primates): Biogeographic and taxonomic implications

The genus Callicebus (Thomas, 1903) is one of the most diverse of Neotropical primate genera and the only extant member of the Callicebinae subfamily. It has a widespread distribution from Colombia to Brazil, Bolivia, Peru and northern Paraguay. Coat colouring and colour pattern vary substantially within the genus, and this has led to the description of numerous species and subspecies, as well as numerous species groups. However, a lack of molecular phylogenetic analyses on the genus means that phylogenetic relationships and biogeographic history of species are poorly understood. Here, we examined phylogenetic relationships and patterns of diversification within the Callicebus cupreus species Group (sensu Kobayashi, 1995) using complete mitochondrial DNA cytochrome b gene sequence. Analyses indicate that the Callicebus cupreus Group underwent recent and extensive diversification. The common ancestor appears to have emerged some 2.3 million years ago (Ma) from a centre of origin in the western Amazon region, followed by diversification of the group between about 1.5 and 1.2Ma. Phylogenetic analyses were able to recover most previously described species (including the recently described Colombian endemic Callicebus caquetensis). However, there are some notable inconsistences between the obtained phylogeny and current taxonomy. Some previously recognized taxa were not separated by our data (e.g., Callicebus caligatus and Callicebus dubius), while currently unrecognized species diversity was uncovered within C. cupreus in the form of two divergent lineages: one of which exhibited greater phylogenetic similarity to species from the C. moloch Group. Based on the present study, we challenge current taxonomic arrangements for the C. cupreus species Group and call for a thorough taxonomic revision within the genus Callicebus.

The Distribution and Taxonomy of Titi Monkeys (Callicebus) in Central and Southern Peru, with the Description of a New Species

Abstract: Here we report on the results of a study on the distribution and taxonomy of titi monkeys, genus Callicebus, in the central part of Peru. We reinstate Callicebus toppini Thomas, a species described in 1914, but since then neglected by science. It evidently has a wide distribution in southern Peru, western Brazil and northern Bolivia. Based on field observations, analysis of museum specimens, and photographs, we also describe a new species of Callicebus from the Rio Urubamba basin, endemic to Peru. Reliable identification of titi monkeys observed in the wild is crucial to avoid confusion and to determine conservation strategies.

Vocal behavior of black‐fronted titi monkeys (Callicebus nigrifrons): Acoustic properties and behavioral contexts of loud calls

Loud calls can be heard over long distances due to their high amplitude and low frequency. These calls are commonly used for both within- and between-group communication in many bird and primate species. In the Neotropics, mated pairs of socially monogamous titi monkeys (genus Callicebus) emit conspicuous, coordinated loud calls. These vocalizations appear to play a role in territorial defense, a hypothesis derived from studies of only three of the 31 recognized Callicebus species. Here, we describe the acoustic properties and organization of the loud calls of black-fronted titi monkeys (Callicebus nigrifrons). We compare the behavioral and ecological contexts associated with these vocalizations to investigate their role in within- and between-group communication, resource defense, and mate defense. Black-fronted titi monkeys create loud calls by combining a finite number of syllables to form more complex phrases, which are assembled to compose long sequences of loud calls. Bioacoustic features distinguish the loud calls used in different contexts, involving communication within- and between-groups. We found support for the hypothesis that vocalizations used for between-group communication are cooperative displays used by the mated pair and other group members to regulate access to important food resources, such as fruits. On the other hand, we only found weak support for the mate defense hypothesis.

New species of titi monkey, genus Callicebus Thomas, 1903 (Primates, Pitheciidae), from Southern Amazonia, Brazil

The genus Callicebus is one of the most diverse Neotropical primate groups, with 31 recognized species. However, large knowledge gaps still exist regarding the diversity of this genus. Such gaps are gradually being filled due to recent intensification of sampling efforts. Several geographic distributions have been better delimited, and six new species have been described in the last 15 years. The goal of the present study is to describe a new species of Callicebus belonging to the Callicebus moloch species group, recently discovered in an area previously considered to be part of the geographic distribution of C. cinerascens. Data collection was conducted through direct observations, specimen collection and interviews with local residents during four expeditions. Specimens were deposited in the mammalian collection of the Museu Paraense Emilio Goeldi.. For a comparative evaluation, we examined specimens of the other species of the Callicebus moloch species group, especially the geographically neighboring forms, C. bernhardi and C. cinerascens. We examined 10 chromatic characters of the fur. In addition to body mass, we verified the conventional external variables and 26 craniometric variables. The new species differs from all other Amazonian Callicebus by an exclusive combination of characters, being easily distinguished by the light gray line of the forehead, dark ocher sideburns and throat, dark gray portions of the torso and flanks, and uniformly orange tail. The geographic distribution of the new species is limited by the Roosevelt and Aripuana rivers, in the states of Mato Grosso and Amazonas, Brazil. Approximately 25% (1,246.382 ha) of this area falls within conservation areas, with five areas of sustainable use (746,818 ha) and three of integral protection (499,564 ha). Furthermore, a considerable portion of the distribution area is located within indigenous lands (1,555.116 ha - 32%). Therefore, 57% (2,801.498 ha) of the occurrence area of the new species falls within protected areas.

Observations of a daytime birthing event in wild titi monkeys (Callicebus oenanthe): implications of the male parental role

Behaviors displayed during birth events, including prenatal, parturition, and postpartum periods, can give insight into caretaking roles in species in which the offspring is cared for by individuals other than the mother. Titi monkeys, genus Callicebus, exhibit a pair-bonded social system along with intense male care of offspring. Here, I report the first case of a birth seen in the wild in a group of Callicebus oenanthe, a little-known species in northern Peru, and describe infant care and development during the first few months after birth. Detailed behavior during the birth sequence as well as ad libitum data postpartum were recorded on nursing and infant care behaviors, including infant carrying, infant grooming, anogenital cleaning, protection, playing, and food sharing. In the 3 h preceding and during parturition, the male remained in contact with or in close proximity to the female (<1 m). The male licked and examined the newborn 3 min after parturition, carried the infant within 24 h after birth, was the main carrier of the infant, and was the predominant manual groomer of the infant during the first 4 months after birth. I argue that the male plays an integral role during the birth in order to establish his bond with the infant as well as reinforce infant care duties to the female and in predator vigilance. In light of various explanations for the exhibition of intense paternal care, I suggest that the male titi monkey provides infant care to release the female of these duties in order that she may spend more time foraging, thus potentially increasing the pair's overall reproductive output.

Two new specimens for the Bolivian endemic titi monkeys, &lt;i&gt;Callicebus olallae&lt;/i&gt; and &lt;i&gt;Callicebus modestus&lt;/i&gt;

No abstract

Insect Prey Foraging Strategies inCallicebus oenanthein NorthernPeru

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.

A new species of Callicebus Thomas, 1903 (Primates, Pitheciidae) from the states of Mato Grosso and Pará, Brazil

A new species of titi monkey, genus Callicebus Thomas, 1903, is described based on four individuals, one from a small tributary of the left bank of Rio Teles Pires, northern state of Mato Grosso, and three others from Largo do Souza, Rio Iriri, Pará, Brazil. The new species belongs to the Callicebus moloch species group, and the main diagnostic characteristics of the new species are the whitish forehead, sideburns and beard coloration, which are contiguous, forming a frame around the blackish face; overall body pelage coloration is pale grayish-brown agouti; hands, feet and tip of the tail whitish; belly and inner sides of fore and hind limbs uniformly orange. The pattern of pelage coloration and qualitative and quantitative skull morphology are described and compared to the other species of the Callicebus moloch group. Species of the Callicebus moloch group show great similarity in skull morphology and morphometrics, making the external morphological characters, specially the chromatic fields, the most reliable diagnostic trait to identify the species.

A morphological analysis of some species of &lt;i&gt;Callicebus, Thomas, 1903 (Pitheciidae - Callicebinae)

A chromogenetic field analysis was performed with 25 of 29 of the known species of the genus Callicebus. Some species presented polymorphism, such as C. moloch, C. hoffmansii and C. cupreus. C. bernhardi presents the same distribution of color in chromogenetic fields as C. moloch, differing only in pigment amount, mainly in ventral surfaces, suggesting C. bernhardi is a junior synonym of C. moloch. C. hoffmansii presents two distinct phenotypes, but without a geographic barrier between them. Callicebus cupreus, C. dubius and C. caligatus are distinct species.

Habitat characterization and population status of the dusky titi (&lt;i&gt;Callicebus ornatos&lt;/i&gt;) in fragmented forests, Meta, Colombia

No abstract

On a New Species of Titi Monkey, Genus Callicebus Thomas (Primates, Pitheciidae), from Western Bolivia with Preliminary Notes on Distribution and Abundance

This paper describes a new species of titi monkey, Callicebus aureipalatii, recently discovered in the Madidi protected area of northwestern Bolivia. Descriptions are based on observations, photographs and video material, and the subsequent collection of two specimens. Preliminary surveys and notes on habitat associations indicate that C. aureipalatii is limited in distribution to the western side of the Río Beni. It is found in the Andean foothills and immediately adjacent lowland forests. Line transect studies at four sites and subsequent extrapolations based on available suitable habitat suggest that population densities are sufficiently high to ensure the protection of this species within the confines of the Madidi protected area. This finding is discussed with reference to the general lack of knowledge regarding titi monkey distributions in Bolivia.

Karyotypic study of Callicebus coimbrai: a rare and threatened primate species from Brazil

The genus Callicebus comprises 28 species distributed in the Amazonia and Atlantic forest biomes. This paper describes the karyotype of C. coimbrai ,a rare and threatened species and compares it with related species (C. personatus and C. nigrifrons). The karyotype was characterized by G-, C-sequential and NOR banding. C. coimbrai presented 2n=44 chromosomes, with G-banding pattern similar to that observed in C. personatus (2n=44) and C. ni- grifrons (2n=42). The karyotypic divergence between C. coimbrai and C. nigrifrons is explained by a single rearrange- ment of centric fusion/fission. The chromosomal data obtained suggest a closer association between C. coimbrai and C. personatus than with C. nigrifrons.

A taxonomic review of the titi monkeys, genus &lt;i&gt;Callicebus&lt;/i&gt; Thomas, 1903, with the description of two new species, &lt;i&gt;Callicebus bernhardi&lt;/i&gt; and &lt;i&gt;Callicebus stephennashi&lt;/i&gt;, from Brazilian Amazonia

&#x0D; &#x0D; &#x0D; This paper provides a taxonomic review of the titi monkeys, genus Callicebus, and describes two new species from central Brazilian Amazonia, Callicebus bernhardi and Callicebus stephennashi. Previous revisions include Hershkovitz (1988, 1990), Kobayashi (1995), Kobayashi and Langguth (1999) and Groves (1993, 2001). Here we arrange the titi monkeys, genus Callicebus Thomas, 1903, into five Species Groups or clades, and a total of 28 species. The Callicebus donacophilus Group is represented by the following species: Callicebus modestus Lönnberg, 1939, Callicebus donacophilus (d’Orbigny, 1836), Callicebus pallescens Thomas, 1907 (treated by Hershkovitz as a subspecies of C. donacophilus), Callicebus olallae Lönnberg, 1939, and Callicebus oenanthe Thomas, 1924. The Callicebus moloch Group is represented by the following species: Callicebus cinerascens (Spix, 1823), Callicebus hoffmannsi Thomas, 1908, Callicebus baptista Lönnberg, 1939 (treated by Hershkovitz as a subspecies of C. hoffmannsi), Callicebus brunneus (Wagner, 1842), Callicebus moloch (Hoffmannsegg, 1807), and the new species here described as Callicebus bernhardi. The Callicebus cupreus Group is represented by the following species: Callicebus cupreus (Spix, 1823), Callicebus discolor (I. Geoffroy &amp; Deville, 1848) (treated by Hershkovitz as a subspecies of C. cupreus), Callicebus ornatus (Gray, 1866) (treated by Hershkovitz as a subspecies of Callicebus cupreus), Callicebus caligatus (Wagner, 1842), Callicebus dubius Hershkovitz, 1988, and the new species here described as Callicebus stephennashi. The Callicebus torquatus Group is represented by the following species: Callicebus torquatus (Hoffmannsegg, 1807), Callicebus lugens (Humboldt, 1811) (treated by Hershkovitz as a subspecies of C. torquatus), Callicebus purinus Thomas, 1927 (treated by Hershkovitz as a subspecies of C. torquatus), Callicebus lucifer Thomas, 1914 (treated by Hershkovitz as a subspecies of C. torquatus), Callicebus regulus Thomas, 1927 (treated by Hershkovitz as a subspecies of C. torquatus), and Callicebus medemi Hershkovitz, 1963 (treated by Hershkovitz as a subspecies of C. torquatus). The Callicebus personatus Group is treated separately from the Callicebus moloch Group and is represented by the following species: Callicebus personatus (É. Geoffroy, 1812), Callicebus melanochir (Wied-Neuwied, 1820) (treated by Hershkovitz as a subspecies of C. personatus), Callicebus nigrifrons (Spix, 1823) (treated by Hershkovitz as a subspecies of C. personatus), Callicebus barbarabrownae Hershkovitz, 1990 (treated by Hershkovitz as a subspecies of C. personatus), and Callicebus coimbrai Kobayashi &amp; Langguth, 1999. Callicebus bernhardi was discovered in the Rio Aripuanã basin in 1996 by M. G. M. van Roosmalen, who also discovered Callicebus stephennashi in 2001, while traveling on the Rio Purus. The geographic distributions of all hitherto recognized Callicebus species are updated, and the validity of the river barrier hypothesis for titis and other Amazonian primates is discussed, along with their conservation status.&#x0D; &#x0D; &#x0D;

A morphological study of upper first and second molars in the genus Callicebus.

The intra- and inter-specific variations in dental characters of three forms of Callicebus were studied: C. torquatus, C. moloch and C. personatus. Although the range of variations overlapped extensively in some traits, their frequencies or degree of development were consistently different among them. Thus, the species-level identification among Callicebus may be safely done.Furthermore, an evolutionary trend of Callicebus was suggested based on the dental morphologies. The trend seems to be represented from the torquatus-type molar to the personatus-type one through the moloch-type's as the succession of morphology. This evolutionary trend was also supported with the result of morphological comparisons between the living Callicebus and the fossil Cebidae monkeys from the middle Miocene.

LV.—New callicebus and Eumops from S. America

LV.—<i>New</i> callicebus <i>and</i> Eumops <i>from S. America</i>