Unique nasal turbinal morphology reveals Homunculus patagonicus functionally converged on modern platyrrhine olfactory sensitivity.

The phyletic position of early Miocene platyrrhine Homunculus patagonicus is currently a matter of debate. Some regard it to be an early member of the Pitheciidae, represented today by the sakis, uakaris, and titi monkeys. Others view Homunculus as a stem platyrrhine, part of a group that diversified in Patagonia and converged in some respects on modern pitheciine dental and gnathic morphology and perhaps seed-eating specialization. New details of its internal nasal anatomy are pertinent to resolving this debate. In addition, they provide a new perspective on how modern platyrrhine olfactory sensitivity evolved. Here we reconstruct the internal nasal anatomy of Homunculus from high-resolution computed tomography scans. This species has three ethmoturbinals, the scrolls of bone in the nasal fossa that were covered in sensory epithelium in vivo. This condition stands in stark contrast to extant platyrrhines, and indeed to all other haplorhines, which have only two ethmoturbinals or, in the case of all pitheciid platyrrhines, only one ethmoturbinal. Quantitatively, however, Homunculus has an olfactory turbinal surface area that falls within the modern platyrrhine distribution, suggesting that while turbinal numbers differ, olfactory sensitivity in this taxon was likely comparable to that of modern platyrrhines. These new data from the fossil record provide further support for the hypothesis that Homunculus is a stem platyrrhine that functionally converged on modern platyrrhines rather than being an early representative of any extant clade.

Dental topographic change with macrowear and dietary inference in Homunculus patagonicus.

Homunculus patagonicus is a stem platyrrhine from the late Early Miocene, high-latitude Santa Cruz Formation, Argentina. Its distribution lies farther south than any extant platyrrhine species. Prior studies on the dietary specialization of Homunculus suggest either a mixed diet of fruit and leaves or a more predominantly fruit-eating diet. To gain further insight into the diet of Homunculus, we examined how the occlusal surfaces of the first and second lower molars of Homunculus change with wear by using three homology-free dental topographic measures: Dirichlet normal energy (DNE), orientation patch count rotated (OPCR), and relief index (RFI). We compared these data with wear series of three extant platyrrhine taxa: the folivorous Alouatta, and the frugivorous Ateles and Callicebus (titi monkeys now in the genus Plecturocebus). Previous studies found Alouatta and Ateles exhibit distinctive patterns of change in occlusal morphology with macrowear, possibly related to the more folivorous diet of the former. Based on previous suggestions that Homunculus was at least partially folivorous, we predicted that changes in dental topographic metrics with wear would follow a pattern more similar to that seen in Alouatta than in Ateles or Callicebus. However, wear-induced changes in Homunculus crown sharpness (DNE) and complexity (OPCR) are more similar to the pattern observed in the frugivorous Ateles and Callicebus. Based on similar wear modalities of the lower molars between Homunculus and Callicebus, we infer that Homunculus had a primarily frugivorous diet. Leaves may have provided an alternative dietary resource to accommodate fluctuation in seasonal fruiting abundance in the high-latitude extratropical environment of late Early Miocene Patagonia.

On a new species of titi monkey (Primates: Plecturocebus Byrne et al., 2016), from Alta Floresta, southern Amazon, Brazil.

The taxonomy of the titi monkeys (Callicebinae) has recently received considerable attention. It is now recognised that this subfamily is composed of three genera with 33 species, seven of them described since 2002. Here, we describe a new species of titi, Plecturocebus, from the municipality of Alta Floresta, Mato Grosso, Brazil. We adopt an integrative taxonomic approach that includes phylogenomic analyses, pelage characters, and locality records. A reduced representation genome-wide approach was employed to assess phylogenetic relationships among species of the eastern Amazonian clade of the Plecturocebus moloch group. Using existing records, we calculated the Extent of Occurrence (EOO) of the new species and estimated future habitat loss for the region based on predictive models. We then evaluated the species' conservation status using the IUCN Red list categories and criteria. The new species presents a unique combination of morphological characters: (1) grey agouti colouration on the crown and dorsal parts; (2) entirely bright red-brown venter; (3) an almost entirely black tail with a pale tip; and (4) light yellow colouration of the hair on the cheeks contrasting with bright red-brown hair on the sides of the face. Our phylogenetic reconstructions based on maximum-likelihood and Bayesian methods revealed well-supported species relationships, with the Alta Floresta taxon as sister to P. moloch + P. vieirai. The species EOO is 10,166,653 ha and we predict a total habitat loss of 86% of its original forest habitat under a "business as usual" scenario in the next 24 years, making the newly discovered titi monkey a Critically Endangered species under the IUCN A3c criterion. We give the new titi monkey a specific epithet based on: (1) clear monophyly of this lineage revealed by robust genomic and mitochondrial data; (2) distinct and diagnosable pelage morphology; and (3) a well-defined geographical distribution with clear separation from other closely related taxa. Urgent conservation measures are needed to safeguard the future of this newly discovered and already critically endangered primate.

Analyzing the sclerocarpy adaptations of the Pitheciidae mandible.

Primates are interpreted to be ancestrally adapted to frugivory, although some modern groups show clear adaptations to other diets. Among them, pitheciids stand out for specifically predating seeds. This dietary specialization is known as sclerocarpy and refers to the extraction of seeds from surrounding hard tissues using the anterior dentition followed by the mastication of seeds by the molars. It has been proposed that Callicebus-Pithecia-Chiropotes-Cacajao represent a morphocline of increasingly specialized anatomical traits for sclerocarpic foraging. This study addresses whether there is a sclerocarpic specialization gradient in the mandibular morphology of pitheciids. Finite element analysis (FEA) was used to simulate two biting scenarios and the obtained stress values were compared between different pitheciids. Geometric morphometrics (GM) were used to display the morphological variation of this group. No support was found for the morphocline hypothesis from a biomechanical viewpoint since all pitheciins showed similar stress values and on average Chiropotes rather than Cacajao exhibited the strongest mandible. From a morphological perspective, it was found that there is indeed relative "robusticity" continuum in the pitheciid mandible for some aspects of shape as expected for the morphocline hypothesis, but this gradient could be related to other factors rather than sclerocarpic specialization. The present results are expected to contribute to a better insight regarding the ecomorphological relationship between mandibular morphology and mechanical performance among pitheciids.

A molar microwear texture analysis of pitheciid primates.

Dental microwear textures have been examined for a broad range of extant primates to assess their efficacy for reconstructing diets of fossil species. To date though, no dental microwear texture data have been published for pitheciid molars, despite reported variation in degree of sclerocarpy and, by extension, the fracture properties of foods these platyrrhines eat. While all pitheciids eat hard or tough seeds, Chiropotes and Pithecia have been documented to consume more than Callicebus. In this study, we explored whether measures of molar microwear texture complexity discriminate taxa following variation in reliance upon seeds, and whether dispersion among variables is greatest in Callicebus, which has the most variable diet. Here we report results for a study of microwear textures on M2 "Phase II" facets of Ch. satanas (N = 14), P. irrorata (N = 8), and Ca. moloch (N = 24) from the Brazilian Amazon (Oriximina, UHE Samuel, and Taperinha, respectively). Textures examined using a scanning confocal profiler showed significant differences in central tendencies for three measures: mean dale area (Sda), anisotropy (Str), and heterogeneity (HAsfc9 ). Ten measures showed significant differences in dispersion, with Callicebus being significantly more variable in eight of those ten. These results demonstrate that the pitheciids with different morphological adaptations and dietary reliance on seeds differ in their dental microwear textures, though less than initially hypothesized. Measures of dispersion, especially, show potential for identifying dietary variability.

Error in geometric morphometric data collection: Combining data from multiple sources.

OBJECTIVES: This study compares two- and three-dimensional morphometric data to determine the extent to which intra- and interobserver and intermethod error influence the outcomes of statistical analyses. MATERIALS AND METHODS: Data were collected five times for each method and observer on 14 anthropoid crania using calipers, a MicroScribe, and 3D models created from NextEngine and microCT scans. ANOVA models were used to examine variance in the linear data at the level of genus, species, specimen, observer, method, and trial. Three-dimensional data were analyzed using geometric morphometric methods; principal components analysis was employed to examine how trials of all specimens were distributed in morphospace and Procrustes distances among trials were calculated and used to generate UPGMA trees to explore whether all trials of the same individual grouped together regardless of observer or method. RESULTS: Most variance in the linear data was at the genus level, with greater variance at the observer than method levels. In the 3D data, interobserver and intermethod error were similar to intraspecific distances among Callicebus cupreus individuals, with interobserver error being higher than intermethod error. Generally, taxa separate well in morphospace, with different trials of the same specimen typically grouping together. However, trials of individuals in the same species overlapped substantially with one another. CONCLUSION: Researchers should be cautious when compiling data from multiple methods and/or observers, especially if analyses are focused on intraspecific variation or closely related species, as in these cases, patterns among individuals may be obscured by interobserver and intermethod error. Conducting interobserver and intermethod reliability assessments prior to the collection of data is recommended.

An Improved Technique Using Dental Prostheses for Field Quantification of the Force Required by Primates for the Dental Penetration of Fruit.

Tooth morphology is an important determinant of primate diet, setting potential limits on processable item size and material properties. Plunger-based commercial fruit firmness testers (penetrometers) have been used to estimate primate diet item hardness and, by proxy, bite force required for penetration. However, geometric forms and surface areas of penetrometer plungers and primate teeth differ considerably. Accurate bite force estimation is especially important with pitheciine primates as these penetrate fruit pericarps with their canines. To achieve more realistic bite force measures, we replaced a fruit penetrometer's standard plunger with a Cacajao calvus canine prosthesis. We compared indentation and penetration values for Hevea spruceana (Euphorbiaceae; hard-pericarp) and Mauritia flexuosa (Arecaceae; soft-pericarp) fruits (both natural Cacajao foods), and standard penetrometer head and canine prosthesis values for penetrating H. spruceana sulci. Compared to the canine prosthesis, a standard head overestimated the force needed to indent and penetrate H. spruceana fruit by more than twofold and, due to greater width, could not effectively penetrate a sulcus: sulcal penetrability data were easily retrieved with the canine prosthesis. We believe this new approach using dental prostheses has potential in the analysis of primate foraging mechanisms, especially for pitheciines for which canines are of paramount importance in accessing food.

1.32 ± 0.11 Ma age for underwater remains constrain antiquity and longevity of the Dominican primate Antillothrix bernensis.

Endemic New World monkeys are an important element of the extinct mammal faunas of the Caribbean's Greater Antilles. Here we report the first geochronometric evidence that the primate Antillothrix bernensis existed in the Dominican Republic during the Pleistocene, based on the uranium-series age of carbonate speleothem that encased a tibia when it was collected in a flooded cave. Three-dimensional geometric morphometrics of laser-scanned living and extinct samples provide evidence to support the hypothesis that this specimen and other Dominican primate tibial remains belong to that same species. U-Th dating of the host cave carbonate returns ages consistently at the 600 ka upper limit of the technique. However, U-Pb, capable of resolving ages of greater antiquity, is more robust in this context, returning a secure age of 1.32 ± 0.11 Ma, which is the oldest chronometric age recorded for a Hispaniolan mammal. While its origins and manner and time of arrival are obscure, the morphometric studies are consistent with phylogenetic analyses that place A. bernensis within the pitheciid clade of the platyrrhines. The species apparently endured for over 1 million years during the climatic perturbations of the Pleistocene, as a frugivorous climbing quadruped, one of two known primate species occupying the hazard prone island of Hispaniola.

µ and κ opioid receptor distribution in the monogamous titi monkey (Callicebus cupreus): implications for social behavior and endocrine functioning.

The opioid system is involved in infant-mother bonds and adult-adult bonds in many species. We have previously shown that µ opioid receptors (MORs) and κ opioid receptors (KORs) are involved in regulating the adult attachment of the monogamous titi monkey. The present study sought to determine the distribution of MOR and KOR in the titi monkey brain using receptor autoradiography. We used [(3)H][D-Ala(2),N-Me-Phe(4),Gly(5)-ol]-enkephalin (DAMGO) to label MORs and [(3)H]U69,593 to label KORs. MOR binding was heterogeneous throughout the titi monkey brain. Specifically, MOR binding was observed in the cingulate gyrus (CG), striatum, septal regions, diagonal band, amygdala, hypothalamus, hippocampus, and thalamus. Binding was particularly dense in the septum, medial amygdala, paraventricular nucleus of the hypothalamus, mediodorsal thalamus with moderate binding in the nucleus accumbens. Consistent with other primate species, MOR were also observed in "neurochemically unique domains of the accumbens and putamen" (NUDAPs). In general KOR binding was more homogenous. KORs were primarily found in the CG, striatum, amygdala and hippocampus. Dense KOR binding was observed in the claustrum. Relative MOR and KOR binding in the titi monkey striatum was similar to other humans and primates, but was much lower compared to rodents. Relative MOR binding in the titi monkey hypothalamus was much greater than that found in rodents. This study was the first to examine MOR and KOR binding in a monogamous primate. The location of these receptors gives insight into where ligands may be acting to regulate social behavior and endocrine function.

Reconsidering the taxonomy of the Black-Faced Uacaris, Cacajao melanocephalus group (Mammalia: Pitheciidae), from the northern Amazon Basin.

The black-faced uacaris are a poorly known group of platyrrhine monkeys from the Rio Negro basin in northwestern Amazonia. Originally described as two distinct species-Cacajao melanocephalus (Humboldt 1812) and Cacajao ouakary (Spix 1823)-from opposite banks of the Negro, they were treated as a single species until the end of the twentieth century, when molecular studies reconfirmed their status as true species. One of these studies not only nominated a third (northern) species, Cacajao ayresi Boubli et al. 2008, but also identified C. ouakary as a junior synonym of C. melanocephalus, resulting in the introduction of a new nomen, Cacajao hosomi Boubli et al. 2008. In the present study, additional evidence on morphological and zoogeographic variables is analyzed, which indicates that C. ouakary should be reinstated, and supports the nomination of a neotype of C. melanocephalus. The molecular and zoogeographic data on the species status of the ayresi form are also re-assessed, leading to the conclusion that, on the basis of the evidence available at the present time, this form should be considered a subspecies of C. melanocephalus. A new taxonomic arrangement is proposed, which recognizes two species, C. ouakary and C. melanocephalus, the latter with two subspecies, C. m. melanocephalus and C. m. ayresi.

Oldest known cranium of a juvenile New World monkey (Early Miocene, Patagonia, Argentina): implications for the taxonomy and the molar eruption pattern of early platyrrhines.

A juvenile cranium of Homunculus patagonicus Ameghino, 1891a from the late Early Miocene of Santa Cruz Province (Argentina) provides the first evidence of developing cranial anatomy for any fossil platyrrhine. The specimen preserves the rostral part of the cranium with deciduous and permanent alveoli and teeth. The dental eruption sequence in the new specimen and a reassessment of eruption patterns in living and fossil platyrrhines suggest that the ancestral platyrrhine pattern of tooth replacement was for the permanent incisors to erupt before M(1), not an accelerated molar eruption (before the incisors) as recently proposed. Two genera and species of Santacrucian monkeys are now generally recognized: H. patagonicus Ameghino, 1891a and Killikaike blakei Tejedor et al., 2006. Taxonomic allocation of Santacrucian monkeys to these species encounters two obstacles: 1) the (now lost) holotype and a recently proposed neotype of H. patagonicus are mandibles from different localities and different geologic members of the Santa Cruz Formation, separated by approximately 0.7 million years, whereas the holotype of K. blakei is a rostral part of a cranium without a mandible; 2) no Santacrucian monkey with associated cranium and mandible has ever been found. Bearing in mind these uncertainties, our examination of the new specimen as well as other cranial specimens of Santacrucian monkeys establishes the overall dental and cranial similarity between the holotype of Killikaike blakei, adult cranial material previously referred to H. patagonicus, and the new juvenile specimen. This leads us to conclude that Killikaike blakei is a junior subjective synonym of H. patagonicus.

Functional morphology of the female genital organs in the peruvian red uakari monkey (Cacajao calvus ucayalii).

Functional morphology may provide important information that could improve methodologies for the diagnosis of the reproductive phase of females, and develop assisted breeding techniques for wildlife. This study examined features of genital organs in 19 Peruvian red uakari monkey (Cacajao calvus ucayalii) females in different reproductive stages, collected from wild animals hunted for food by rural communities in the North-eastern Peruvian Amazon, in order to provide knowledge on the reproductive physiology of this species. The observed mean ovulation rate was 1.4 follicles, and the observed maximal follicle diameter was 0.8 cm. After ovulation, the matured follicle luteinizes resulting in functional CL. In case of oocyte fertilization, the pregnancy CL grows to a maximum of 1.2 cm in diameter, and luteal volume per female decreases related to the advance of pregnancy. Pregnant females also present follicular activity until late pregnancy, but non-ovulated follicles do not undergo atretic processes and apparently transform to accessory CL, resulting in a contribution of 30% of the total luteal volume. All pregnant females delivered a single fetus at term, resulting in a rate of reproductive wastage of 20% of oocytes or embryos. The endometrium and the endometrial glands in non-pregnant females in the follicular phase show a significant increase related to the follicular growth, reaching a high proliferation in non-pregnant females in the luteal phase. The red uakari monkey showed different vaginal epithelium features in accordance with the reproductive state of the female, suggesting that vaginal cytology could be a successful methodology with which to characterize the estrous cycle of this species. The present reproductive evaluation of the Peruvian red uakari monkey provides important information that could improve the development of assisted reproductive techniques in non-human primates.

Diet and dental topography in pitheciine seed predators.

Pitheciines (Pithecia, Chiropotes, and Cacajao) are a specialized clade of Neotropical seed predators that exhibit postcanine teeth with low and rounded cusps and highly crenulated occlusal surface enamel. Data on feeding ecology show that Pithecia consumes proportionally more leaves than other pitheciine species, and comparative studies demonstrate its greater molar relief and relative shearing potential. However, data on pitheciine food mechanics show that Pithecia masticates seeds with greater crushing resistance than those preferred by Chiropotes. This variation predicts an opposing morphology characterized by low and more rounded occlusal surfaces in Pithecia. We build on previous research using new methods for molar surface shape quantification by examining pitheciine second molar shearing crest length, occlusal relief, surface complexity, and surface curvature relative to nonseed specializing platyrrhines and within the context of the observed interspecific variation in pitheciine feeding ecology. Consistent with the previous analyses, our findings demonstrate that pitheciine molars exhibit low shearing, relief, and curvature compared with nonseed predators, independent of phylogeny. Pitheciines also exhibit highly "complex" occlusal topography that promotes the efficient breakdown of tough seed tissues. Overall, Pithecia, Chiropotes, and Cacajao share a similar topographic pattern, suggesting adaptation to foods with similar structural and/or mechanical properties. However, Cacajao differs in surface complexity, which reflects some variation in its feeding ecology. Contrary to the predictions, Pithecia and Chiropotes do not differ in any of the topographic variables examined. The range of demands imposed on the postcanine teeth of Pithecia might therefore select for an average topography, one that converges on that of Chiropotes.

Tail architecture and function of Cebupithecia sarmientoi, a Middle Miocene platyrrhine from La Venta, Colombia.

Cebupithecia sarmientoi, an early pitheciine from the Middle Miocene of La Venta, Colombia, preserves an almost complete caudal vertebral sequence (18 vertebrae). Behavioral reconstructions for this taxon based on appendicular elements suggest a locomotor profile similar to that of Pithecia for which vertical clinging postures and leaping behavior are frequently adopted. General tail morphology suggests some similarity with prehensile-tailed Cebus in the proximal tail region, although overwhelming similarity with nonprehensile-tailed Pithecia is evident in the distal tail region. Indices of caudal muscle attachment sites show marked similarities to nonprehensile-tailed platyrrhines, especially Pithecia. However, the cortices of Cebupithecia caudal vertebral bodies are thicker than those of most other nonprehensile-tailed New World primates. Mechanically, this would provide high resistance to bending and torsional stresses, falling within the range exhibited by prehensile-tailed monkeys. These results suggest that Cebupithecia may have employed its tail differently than most nonprehensile-tailed platyrrhines living today, behaviors that possibly involved tail-bracing or twisting during hindlimb (pedal grasping) suspensory behaviors. Such behaviors may serve as a preadaptive model for the full-fledged evolution of below-branch tail suspension and prehensility seen in other New World primates.

Technical note: a landmark-based approach to the study of the ear ossicles using ultra-high-resolution X-ray computed tomography data.

Previous study of the ear ossicles in Primates has demonstrated that they vary on both functional and phylogenetic bases. Such studies have generally employed two-dimensional linear measurements rather than three-dimensional data. The availability of Ultra- high-resolution X-ray computed tomography (UhrCT) has made it possible to accurately image the ossicles so that broadly accepted methodologies for acquiring and studying morphometric data can be applied. Using UhrCT data also allows for the ossicular chain to be studied in anatomical position, so that it is possible to consider the spatial and size relationships of all three bones. One issue impeding the morphometric study of the ear ossicles is a lack of broadly recognized landmarks. Distinguishing landmarks on the ossicles is difficult in part because there are only two areas of articulation in the ossicular chain, one of which (the malleus/incus articulation) has a complex three-dimensional form. A measurement error study is presented demonstrating that a suite of 16 landmarks can be precisely located on reconstructions of the ossicles from UhrCT data. Estimates of measurement error showed that most landmarks were highly replicable, with an average CV for associated interlandmark distances of less than 3%. The positions of these landmarks are chosen to reflect not only the overall shape of the bones in the chain and their relative positions, but also functional parameters. This study should provide a basis for further examination of the smallest bones in the body in three dimensions.

First skull of Antillothrix bernensis, an extinct relict monkey from the Dominican Republic.

The nearly pristine remains of Antillothrix bernensis, a capuchin-sized (Cebus) extinct platyrrhine from the Dominican Republic, have been found submerged in an underwater cave. This represents the first specimen of an extinct Caribbean primate with diagnostic craniodental and skeletal parts in association, only the second example of a skull from the region, and one of the most complete specimens of a fossil platyrrhine cranium yet discovered. Cranially, it closely resembles living cebines but is more conservative. Dentally, it is less bunodont and more primitive than Cebus, with crowns resembling Saimiri (squirrel monkeys) and one of the oldest definitive cebines, the late Early Miocene Killikaike blakei from Argentina. The tricuspid second molar also resembles the enigmatic marmosets and tamarins, whose origins continue to present a major gap in knowledge of primate evolution. While the femur is oddly short and stout, the ulna, though more robust, compares well with Cebus. As a member of the cebid clade, Antillothrix demonstrates that insular Caribbean monkeys are not monophyletically related and may not be the product of a single colonizing event. Antillothrix bernensis is an intriguing mosaic whose primitive characters are consistent with an early origin, possibly antedating the assembly of the modern primate fauna in greater Amazonia during the La Venta horizon. While most Greater Antillean primate specimens are quite young geologically, this vanished radiation, known from Cuba (Paralouatta) and Jamaica (Xenothrix) as well as Hispaniola, appears to be composed of long-lived lineages like several other mainland clades.

Brief communication: Contributions of enamel-dentine junction shape and enamel deposition to primate molar crown complexity.

Molar crown morphology varies among primates from relatively simple in some taxa to more complex in others, with such variability having both functional and taxonomic significance. In addition to the primary cusps, crown surface complexity derives from the presence of crests, cuspules, and crenulations. Developmentally, this complexity results from the deposition of an enamel cap over a basement membrane (the morphology of which is preserved as the enamel-dentine junction, or EDJ, in fully formed teeth). However, the relative contribution of the enamel cap and the EDJ to molar crown complexity is poorly characterized. In this study we examine the complexity of the EDJ and enamel surface of a broad sample of primate (including fossil hominin) lower molars through the application of micro-computed tomography and dental topographic analysis. Surface complexity of the EDJ and outer enamel surface (OES) is quantified by first mapping, and then summing, the total number of discrete surface orientation patches. We investigate the relative contribution of the EDJ and enamel cap to crown complexity by assessing the correlation in patch counts between the EDJ and OES within taxa and within individual teeth. We identify three patterns of EDJ/OES complexity which demonstrate that both crown patterning early in development and the subsequent deposition of the enamel cap contribute to overall crown complexity in primates.

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.