Gut morphology of Callithrix nigriceps and Saguinus labiatus from western Brazilian Amazonia

Quantitative data on the gut proportions of the recently-described black-headed marmoset (Callithrix nigriceps) from western Brazilian Amazonian are presented. Like other marmosets, C. nigriceps exhibits a relatively large caecum and colon associated with adaptations for gummivory. The degree of gut specialisation recorded is greater than that for any other platyrrhine for which quantitative data are available. Gum was found in the stomach contents of all four individuals examined, although the fruit/seeds of as many as seven different plant taxa were also encountered, in addition to insects of six different orders. Gut proportions of two Saguinus labiatus from the same region were typical of the more frugivorous tamarins, and stomach contents included only fruit and insects. Relative gut proportions of both species were closely similar to those of congeners from the same region. © 1993 Wiley-Liss, Inc.     

Foraging behavior of a tamarin group (Saguinus fuscicollis weddelli) and interactions with marmosets (Callithrix emiliae)

We present data on aspects of the behavioral ecology of a free- ranging group of Saguinus fuscicollis weddelliat a site in Brazilian Amazonia where a second callitrichid, Callithrix emiliae,is syntopic. Diet, activity patterns, and ranging behavior are broadly similar to those of S. fuscicollisfrom sites in Bolivia, Brazil, and Perú, though significant seasonal changes include an extreme and atypical form of ranging behavior in which they foraged in central-place fashion around a source of exudate—Parkia pendula. S. f. weddelliwas active at relatively low levels in the forest both in absolute terms and relative to C.emiliae, which appears to be an important factor in their niche partitioning. Association between the two species appeared to be less systematic overall than those observed between S. fuscicollisand congeners at other sites, though this may be partly a result of observation conditions. During the period of central-place foraging, the two species exhibited a high degree of association. Other characteristics of the behavior of S. f. weddelliat the study site include the frequent use of tree holes as sleeping sites.     

Gelatin as a vehicle for food and vitamin administration to marmosets

For a period of three years, gelatin was used as a vehicle for administration of food, vitamin complex and drugs to laboratory maintained Callithrix penicillata and Callithrix jacchus marmosets and a breeding colony of C. penicillata. In both circumstances, results were satisfactory. The animals survived for long periods of time, with adult, young and juvenile primates in the breeding colony showing good physical condition.     

Colour discrimination in the black-tufted-ear marmoset (Callithrix penicillata): ecological implications

The dietary diversity of marmosets is substantial, which may reflect differences in their colour vision. This study examined the colour discrimination ability of a gummivore/insectivore callitrichid, Callithrix penicillata, which inhabits the Brazilian cerrado (bush savanna). A series of ecologically relevant tasks, involving a behavioural paradigm of discrimination learning in semi-natural conditions and the usage of ecologically relevant stimuli, was executed. Three marmosets, 2 males and a female, behaved like human dichromats, showing an impaired performance when orange and green stimuli had to be discriminated. In contrast, 2 females resembled human trichromats, discriminating those kinds of pairs. Our data suggest that Callithrix penicillata presents a polymorphic trichromacy, with dichromatic males and dichromatic or trichromatic females.     

The place of Callimico goeldii in the Callitrichine phylogenetic tree: evidence from von Willebrand factor gene intron II sequences

Sequences of a 0.9-kb DNA segment spanning intron 11 of the von Willebrand Factor gene (vWF) were determined for 21 individuals of 19 primate species. The results of maximum parsimony and maximum likelihood analyses of these vWF sequences are congruent with previous molecular findings from other nonlinked nuclear genomic loci which divide the platyrrhine superfamily Ceboidea into three monophyletic families: Cebidae, Atelidae, and Pitheciidae. The vWF results strongly support the taxon Callitrichinae as a monophyletic subfamily within Cebidae. The four extant callitrichine genera constitute tribe Callitrichini, and the basal branchings within this tribe first separate out Saguinus (tamarins), next Leontopithecus (lion tamarins), and last the sister genera Callimico (Goeldi's monkeys) and Callithrix (marmosets). Callithrix divides into three subclades, with pygmy marmosets (C. pygmaea) as sister of the C. argentata species group and with the C. jacchus species group as their sister. Fossil and DNA evidence place the emergence of the callitrichine clade in the basal cebid radiation at about 20 Ma (million years ago) and the three basal branchings in the callitrichin radiation at about 13 to 11 Ma. In turn, the branchings separating the three subclades of Callithrix are placed at about 5 to 4 Ma.     

Social Change Affects Vocal Structure in a Callitrichid Primate (Callithrix kuhlii)

Vocal plasticity in the face of changing social context is well‐documented in passerine birds, but the degree to which changes in social environment affect the vocal structure of non‐human primates is a topic which has remained largely unexplored. We assessed whether modification of social environments, in this case the presence of marmosets in neighboring cages, influenced the vocal morphology of phee calls, which possess ‘signature’‐like features, in Wied's black tufted‐ear marmosets (Callithrix kuhlii). Individual phee calls were obtained over a period of 8 wk from 11 animals maintained in rooms with stable social environments. After this baseline phase, seven marmosets were housed for an additional 8 wk in rooms that contained cages with unfamiliar marmosets, while four marmosets maintained the same neighbors as the first phase. Calls were digitized and both frequency and temporal parameters were measured. Multivariate discriminant function analyses (DFA) generated from vocalizations collected in the first phase produced functions that accurately classified calls to the correct individual, showing that calls had significant individual distinctiveness. DFAs generated from vocalizations in the first phase of the study continued to show high classification accuracy for marmosets in a stable social environment, but DFAs from the first phase were significantly less likely to correctly classify vocalizations in marmosets that were housed next to novel conspecifics. These data show that phee calls, which have signature‐like properties in marmosets, can be modified by changes in social context. The results suggest a degree of plasticity in vocal signals that is rare among non‐human primates.     

Mitochondrial COII gene sequences provide new insights into the phylogeny of marmoset species groups (Callitrichidae,Primates)

Mitochondrial cytochrome oxidase II (COII) gene sequences (549 base pairs) were used to investigate the taxonomic relationships among 12 marmoset (Callithrix, Cebuella and Mico) taxa. A large number of substitutions were found in the third base codon positions, providing a strong phylogenetic signal in a gene coding a conserved protein. Despite the significant affinity between the 2 Amazonian genera Cebuella and Mico, found in recent molecular studies, the analysis presented here did not resolve convincingly the phylogenetic relationships between the 3 genera. Mico nevertheless formed 3 distinct clades, reflecting a basic division of species groups based on geographic distribution (east or west of the Rio Tapajós) rather than morphology (presence or absence of auricular hair). This supports the taxonomic distinction of the allopatric emiliae forms. In Callithrix, Callithrix aurita forms a distinct clade, but the remaining morphotypes form a somewhat contradictory cluster, possibly resulting from an extremely rapid radiation.     

Hybridization effects and genetic diversity of the common and black‐tufted marmoset (Callithrix jacchus and Callithrix penicillata) mitochondrial control region

Hybridization is continually documented in primates, but effects of natural and anthropogenic hybridization on biodiversity are still unclear and differentiating between these contexts remains challenging in regards to primate evolution and conservation. Here, we examine hybridization effects on the mitochondrial DNA (mtDNA) control region of Callithrix marmosets, which provide a unique glimpse into interspecific mating under distinct anthropogenic and natural conditions. DNA was sampled from 40 marmosets along a 50‐km transect from a previously uncharacterized hybrid zone in NE Brazil between the ranges of Callithrix jacchus and Callithrix penicillata. DNA was also collected from 46 marmosets along a 30‐km transect in a hybrid zone in Rio de Janeiro state, Brazil, where exotic marmosets appeared in the 1980s. Combining Callithrix DNA sampled inside and outside of these hybrid zones, phylogenetic and network analyses show C. jacchus and C. penicillata being parental species to sampled hybrids. We expand limited Callithrix population genetics work by describing mtDNA diversity and demographic history of these parental species. We show ancient population expansion in C. jacchus and historically constant population size in C. penicillata, with the latter being more genetically diverse than the former. The natural hybrid zone contained higher genetic diversity relative to the anthropogenic zone. While our data suggest hybrid swarm formation within the anthropogenic zone due to removed physical reproductive barriers, this pattern is not seen in the natural hybrid zone. These results suggest different genetic dynamics within natural and anthropogenic hybridization contexts that carry important implications for primate evolution and conservation. Am J Phys Anthropol 155:522–536, 2014. © 2014 Wiley Periodicals, Inc.     

Behavioral tests as indicator for pain and distress in a primate endometriosis model

Background As common marmosets (Callithrix jacchus) are frequently used experimental animals, sensitive test systems are needed to evaluate impairment and pain caused by procedures and diseases. Methods A diurnal profile of healthy animals was obtained by videotaping. Differences in social behavior and cognitive skills between marmosets with established endometriosis and healthy monkeys were investigated using the videotaping, the Wisconsin General Test Apparatus (WGTA), and a food tree. Results The marmosets showed a mostly trimodal course of activity. Social grooming and activity were significantly decreased in animals with endometriosis; furthermore, the diseased monkeys habituated significantly worse to the cognitive test settings. The food tree experiments offered no differences between diseased and control animals. Conclusion The videotaping and the WGTA are suitable methods to detect disease‐related impairments in common marmosets, which is essential for the refinement of experiments.     

Physical Environmental Effects on Infant Care and Development in Captive Callithrix jacchus

Environmental enrichment may affect infant care and development in captive primates. We investigated the effects of this factor in laboratory common marmosets (Callithrix jacchus). An enriched physical environment enhanced the social activities of the marmosets and elicited a greater repertoire of behaviors, without negatively affecting the provision of infant care. In addition, infants in enriched cages displayed certain behaviors sooner than infants in non-enriched cages did, which suggests an increased developmental rate. Infants in enriched cages also ate more solid food and engaged in solitary play and exploration more than ones in non-enriched cages did. Play and exploration probably improve spatial cognition and motor skills, which, together with a higher degree of independence, may allow infants to cope better with laboratory routines and general social interactions later in life than their counterparts reared in less complex enclosures. We conclude that laboratories can significantly increase the welfare of marmosets by providing a more complex physical environment.     

Anaesthesia of the common marmoset (Callithrix jacchus) using continuous intravenous infusion of alphaxalone/alphadalone

A safe means of anaesthetizing common marmosets (Callithrix jacchus) for a study using magnetic resonance imaging (MRI) to investigate cerebral ischaemia was required. Continuous infusion of alphaxalone/alphadalone was used to anaesthetize 37 marmosets for non-recovery and recovery experiments. This was found to give safe, reliable anaesthesia when coupled with pulse oximetry and electrocardiographic (ECG) monitoring.     

The establishment of specified-pathogen-free marmosets, Callithrix jacchus.

The establishment of 3 specified-pathogen-free marmosets (Callithrix jacchus) during the period May 1969 to January 1973 is described. A brief history of the conventional breeding colony from which the animals were derived is given and hysterotomy and hand-rearing techniques are described.     

Investigation of marmoset hybrids (Cebuella pygmaea x Callithrix jacchus) and related Callitrichinae (Platyrrhini) by cross-species chromosome painting and comparative genomic hybridization

We report on the cytogenetics of twin offspring from an interspecies cross in marmosets (Callitrichinae, Platyrrhini), resulting from a pairing between a female Common marmoset (Callithrix jacchus, 2n = 46) and a male Pygmy marmoset (Cebuella pygmaea, 2n = 44). We analyzed their karyotypes by multi-directional chromosome painting employing human, Saguinus oedipus and Lagothrix lagothricha chromosome-specific probes. Both hybrid individuals had a karyotype with a diploid chromosome number of 2n = 45. As a complementary tool, interspecies comparative genomic hybridization (iCGH) was performed in order to screen for genomic imbalances between the hybrids and their parental species, and between Callithrix argentata and S. oedipus, respectively. These genomic imbalances were confined to centromeric and telomeric heterochromatin, while euchromatic chromosome regions appeared balanced in all species investigated. When comparing marmosets and tamarins, sequence divergence of centromeric heterochromatin was already clearly noticeable. In the C. argentata and C. pygmaea genomes numerous subtelomeric regions were affected by amplification of different repetitive sequences. Cross-species FISH with a microdissection-derived C. pygmaea repetitive probe revealed species specificity of this repetitive sequence at the molecular cytogenetic level of resolution.     

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

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

Identification of Helicobacter sp. in gastric mucosa from captive marmosets (Callithrix sp.; callitrichidae, primates)

The aim of this study was to identify the presence of Helicobacter sp. in the gastric mucosa of captive marmosets (Callithrix sp.). Histologic specimens from the fundic, corpus, and antral gastric regions of six Callithrix jacchus, 12 C. kuhli, and 12 C. geoffroyi specimens were evaluated. The sections were stained with hematoxylin-eosin (H&E) and the Warthin-Starry silver impregnation method, and immunostained with rabbit anti-H. pylori polyclonal antibody. Helicobacter-like organisms (HLOs) and coccoid forms were present in silver-stained sections from 29 stomachs, whereas immunohistochemistry (IHC) tests revealed bacterial aggregates in 15 stomachs. No statistical difference relative to the presence of Helicobacter sp. was found among the gastric regions or marmoset species. Gastric lesions were found in the groups of marmosets that had positive and negative IHC results, but no correlation between inflammation and Helicobacter sp. infection was established. These findings demonstrate that marmosets are susceptible to naturally-occurring Helicobacter sp. infection, and open the way to the development of comparative studies on Helicobacter sp. infection in humans.     

Saliva sampling to assess cortisol levels in unrestrained common marmosets and the effect of behavioral stress

We report a method for taking saliva samples from unrestrained, captive marmosets (Callithrix jacchus) to assess levels of free cortisol. Saliva samples can be obtained reliably, without any habituation, by encouraging the marmosets to lick and chew a cotton-wool bud coated in banana. Saliva is thus left on the bud. We also tested sweetened fruit-drink crystals and a number of other substances, but none of these attracted all of the marmosets, and even flavors that were effective once soon lost their attraction. The presence of banana in the samples collected was found to lower the measured concentration of cortisol; however, as shown in samples taken with and without the banana coating on the bud, it did so in a linear and consistent way, and did not vary significantly among subjects. Therefore, a simple conversion factor could be applied to correct for the presence of banana. A first experiment showed that the marmosets exhibited a rise in salivary cortisol levels in response to social isolation. A second experiment showed elevation of cortisol during a period when the marmosets were disturbed by increased human activity and noise levels in the building in which they were housed. Hence, this method of saliva sampling is a convenient, noninvasive means of assessing cortisol levels in marmosets.     

Radiographic evaluation of neonatal skeletal development in Callimico goeldii reveals closer similarity to Callithrix jacchus than to Saguinus oedipus

The phylogenetic affinities of the neotropical Goeldi's monkey (Callimico goeldii) have long been a matter of debate. Whereas most morphological evidence appears to place Callimico in a sister group position relative to the Callitrichidae, genetic studies place C. goeldii within the Callitrichidae and suggest that it is more closely related to marmosets than to tamarins. The present study presents the first radiographic analysis comparing the secondary limb bone ossification of newborn C. goeldii with representatives of the marmosets (Callithrix jacchus) and tamarins (Saguinus oedipus). The state of secondary ossification of the epiphysis and short bones is classified into three different ontogenetic stages. Our results reveal that in terms of the number of ossification centers, C. goeldii is significantly closer to C. jacchus than to S. oedipus. This is the first morphological study to support the findings of molecular studies, and the results suggest that C. goeldii is more closely related to marmosets than to tamarins.     

Expression of taste signal transduction molecules in the caecum of common marmosets

The extraoral presence of taste signal transduction proteins has recently been reported in rodents and humans. Here, we report for the first time the presence of these signal transduction proteins in the caecum of a non-human primate, the common marmoset. Quantitative RT-PCR data on the gene expression of taste signal transduction molecules (gustducin and TRPM5) in common marmosets suggested high expression in the caecum, which was not observed in other non-human primates. Immunohistochemical analysis confirmed the specific presence of gustducin and taste receptors in marmoset caecal cells. These results may relate to the specific feeding behaviour of marmosets, which consume plant exudates, primarily gums.     

Characterization of the expressed immunoglobulin IGHV repertoire in the New World marmoset Callithrix jacchus

The common marmoset (Callithrix jacchus jacchus) is a member of the Callithrichinae, a family of outbred New World primates with limited MHC polymorphisms and a propensity to develop spontaneous or experimentally induced autoimmunity. C. jacchus marmosets are susceptible to experimental allergic encephalomyelitis (EAE), and spontaneously develop autoimmune colitis and thyroiditis. Such disease models approximate the complexity of human autoimmune disorders, and allow an investigation of the respective roles of T-cell and antibody responses to self-antigens in outbred species. A key issue for further definition of the pathogenic antibody responses in human autoimmunity is to understand the diversity of the immunoglobulin repertoire in primate models. Here, we characterized the expressed immunoglobulin IGHV repertoire of the C. jacchus marmoset. Six IGHV subgroups were identified which show a high degree of sequence similarity to their human IGHV counterparts (IGHV1, IGHV3, IGHV4, IGHV5, IGHV6, and IGHV7). As in the expressed human IGHV repertoire, the framework regions are more conserved when compared to the complementarity-determining regions (CDRs), with the greatest degree of variability located in CDR3. Predicted structural features are highly conserved between C. jacchus and human IGHV. This information now provides a framework for studies of the antigen-specific repertoire of pathogenic antibodies in EAE and other immune-mediated diseases.     

Variation in circulating and excreted estradiol associated with testicular activity in male marmosets.

Concentrations of estradiol (E2) are high in the urine of male marmosets, and links between E2 and paternal behavior have been proposed in black tufted-ear marmosets, Callithrix kuhlii. However, it is not clear whether urinary E2 in male marmosets: 1) represents production of E2 associated with testicular activity, 2) is associated with adrenal steroid production, or 3) merely reflects peripheral conversion of T to E2 prior to excretion. We tested the hypothesis that urinary E2 in male marmosets represents estrogen production-associated activity in the hypothalamus-pituitary-gonad (HPG) axis. We treated adult male marmosets with gonadotropin-releasing hormone (GnRH), and used saline-treated males as controls. We collected blood and urine samples from males before and after treatment, and assayed them for testosterone (T), estradiol (E2), and cortisol (CORT). Treatment with GnRH increased circulating T and E2, and prevented decreases in levels of urinary T and E2. Moreover, changes in plasma and urinary E2 after treatment were positively correlated with post-treatment changes in T. Thus, our data are consistent with both plasma and urinary E2 in male marmosets increasing as a result of testicular stimulation. However, treatment with GnRH did not affect plasma or urinary CORT concentrations of males, suggesting that the E2 excreted by males is not of adrenal origin. We also compared urinary T, E2, and CORT levels between intact and castrated male common marmosets (Callithrix jacchus). Urinary concentrations of T and E2, but not CORT, were significantly lower in castrated than in intact males, further suggesting that E2 in male marmosets varies with testicular activity.