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.     

Molecular cytotaxonomy of New World monkeys (Platyrrhini) - comparative analysis of five species by multi-color chromosome painting gives evidence for a classification of Callimico goeldii within the family of Callitrichidae

Chromosome rearrangements are considered as "rare genomic changes" and can provide useful markers and even landmarks for reconstructing phylogenies complementary to DNA sequence data and bio-morphological comparisons. Here, we applied multi-directional chromosome painting to reconstruct the chromosome phylogeny and evolutionary relationships among the New World monkey (Platyrrhini) species Callithrix argentata, Cebuella pygmaea, Saguinus oedipus, Callithrix jacchus and Callimico goeldii. The results clarified several aspects of New Wold monkey phylogeny. In particular the phylogenetic position of C. goeldii was elucidated, which has been controversially discussed and variously classified in the family Callitrichidae, in the family Cebidae or in its own family Callimiconidae. Comparative genome maps were established by multi-color fluorescence in situ hybridization (FISH) with human, S. oedipus and Lagothrix lagothricha chromosome- specific DNA probes. From these data we reconstructed the putative ancestral karyotype of all Callitrichidae. Various derived chromosomal syntenies are shared by all five species and cytogenetically define Callitrichidae - including Callimico goeldii -- as a distinctive group within the Platyrrhini. C. pygmaea and C. argentata share identical chromosomal syntenies from which S. oedipus and C. jacchus differ by single independent translocations. A common derived chromosomal change links Callimico with the marmosets to the exclusion of the tamarins, however, it has further diverged from an ancestral marmoset karyotype by at least four apomorphic rearrangements. Saimiri sciureus, representing the Cebinae, exclusively shares a derived syntenic association with all Callithrichidae, defining the genus Saimiri as a sister group.     

Comparative analysis of masseter fiber architecture in tree-gouging (Callithrix jacchus) and nongouging (Saguinus oedipus) callitrichids

Common marmosets (Callithrix jacchus) and cotton-top tamarins (Saguinus oedipus) (Callitrichidae, Primates) share a broadly similar diet of fruits, insects, and tree exudates. Common marmosets, however, differ from tamarins by actively gouging trees with their anterior teeth to elicit tree exudate flow. During tree gouging, marmosets produce relatively large jaw gapes, but do not necessarily produce relatively large bite forces at the anterior teeth. We compared the fiber architecture of the masseter muscle in tree-gouging Callithrix jacchus (n = 10) to nongouging Saguinus oedipus (n = 8) to determine whether the marmoset masseter facilitates producing these large gapes during tree gouging. We predict that the marmoset masseter has relatively longer fibers and, hence, greater potential muscle excursion (i.e., a greater range of motion through increased muscle stretch). Conversely, because of the expected trade-off between excursion and force production in muscle architecture, we predict that the cotton-top tamarin masseter has more pinnate fibers and increased physiological cross-sectional area (PCSA) as compared to common marmosets. Likewise, the S. oedipus masseter is predicted to have a greater proportion of tendon relative to muscle fiber as compared to the common marmoset masseter. Common marmosets have absolutely and relatively longer masseter fibers than cotton-top tamarins. Given that fiber length is directly proportional to muscle excursion and by extension contraction velocity, this result suggests that marmosets have masseters designed for relatively greater stretching and, hence, larger gapes. Conversely, the cotton-top tamarin masseter has a greater angle of pinnation (but not significantly so), larger PCSA, and higher proportion of tendon. The significantly larger PCSA in the tamarin masseter suggests that their masseter has relatively greater force production capabilities as compared to marmosets. Collectively, these results suggest that the fiber architecture of the common marmoset masseter is part of a suite of features of the masticatory apparatus that facilitates the production of relatively large gapes during tree gouging.     

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.     

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.     

Reproductive performance of three species of Callitrichidae

The reproductive performance of three species of Callitrichidae housed under identical conditions, including relatively spacious caging and visual screening, was compared. The three species were Callithrix jacchus, Saguinus fuscicollis, and Saguinus oedipus. Callithrix jacchus was the most reliable breeder, with the lowest percentage of stillborn and the highest post-weaning survival. While the reproductive performance of S oedipus was better than that generally reported for other colonies, the reproductive performance of the Saguinus species was still poorer than that of C jacchus. The two Saguinus species did not differ significantly in either percentage of stillborn or post-weaning survival. None of the species showed infertility due to lactation, but the mean inter-birth interval was significantly longer for S oedipus than for either C jacchus or S fuscicollis.     

Matrilineal genetic structure within and among populations of the cooperatively breeding common marmoset,Callithrix jacchus

Common marmosets are members of the family Callitrichidae, South American primates characterized by highly social group living and cooperative breeding. In this study we analysed 1112 base pairs (bp) of the mitochondrial control region in 59 Callithrix jacchus individuals, sampled mainly from two geographically distinct field sites in N.E. Brazil. Analysis of molecular variation revealed a highly significant genetic structuring of haplotypes between social groups and between populations. Examination of matrilineal genetic structure within social groups revealed that seven of nine recorded breeding pairs were from different maternal lineages, indicating assortative mating and outbreeding. In addition to the breeders, at least six of 10 groups contained adult individuals from different matrilines, with five haplotypes present in one social group of nine animals. Groups of mixed lineages raise questions about potential reproductive conflicts of interest, and the extent of kin-selected altruism in the evolution and maintenance of cooperative breeding in this species.     

“Environmental stress” and reproductive success in the common marmoset (Callithrix jacchus jacchus)

The present report documents the breeding success of a new colony of common marmosets (Callithrix jacchus jacchus) and demonstrates a correlation between environmental stress and reproductive success. Environmental conditions ranged chronologically over 40 months, through four periods: I) the initial period, when the colony was formed; II) a phase of relative environmental stability; III) a stage of “environmental stress” (when the colony was disrupted by nearby construction); and IV) a return to a stable environment. Examination of reproductive status during each period indicated that the colony exhibited severe reproductive suppression during the time of the environmental disruption. Parity and the number of live births decreased and the number of spontaneous abortions increased during this period. Reproductive success remained low during period IV. More triplets than twins were born during the period of relative environmental stability.     

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.     

Home-range size and use and territorial behavior in the common marmoset,Callithrix jacchus jacchus,at the tapacura field station,recife, Brazil

Data were obtained both from observation and by radiolocation on the size and use of the home range of the common marmoset, Callithrix jacchus jacchus.Ranges were small compared to those of other callitrichids, varying between 0.72 to 1.62 ha, and a high proportion of the home range was used each day. The marmosets showed territorial behavior, defending an area almost equivalent to the home range. Despite this, mating between animals belonging to neighboring groups was seen. Correlations between the use of the home range and some environmental variables showed little consistency between two groups which occupied ranges of differing resource density, and their activity patterns, as measured by movement through their ranges, were also different. Possible reasons for these inconsistencies are discussed.     

Successful infection of the common marmoset (Callithrix jacchus) with human varicella-zoster virus.

The common marmoset, Callithrix jacchus, can be infected with human varicella-zoster virus (VZV), both wild-type strain KMcC and attenuated vaccine strain Oka/Merck. Infection was accomplished with either whole-cell-associated or cell extract VZV by combined oral-nasal-conjunctival application and was characterized by substantial and persistent anti-VZV antibody responses. The infectivity of VZV for marmosets was destroyed by treatment of inocula with heat or UV light. Diluted inocula with as few as 40 PFU/ml were infectious for marmosets. The lungs were demonstrated to be a major site of viral replication; both the presence of viral antigens and signs of pneumonia were demonstrated in lung tissues. Four serial passages of VZV KMcC were carried out in C. jacchus by a process of in vitro isolation and culturing of VZV from infected lung tissue and reapplication of the cultured isolates to fresh animals. The isolated viruses were identified as VZV both serologically and by restriction endonuclease analyses. The C. jacchus infectivity model should prove useful for determining the efficacy of subunit and live recombinant VZV vaccines as well as for the study of zoster.     

Poxvirus infection in a colony of common marmosets (Callithrix jacchus)

An epizootic poxvirus infection occurred in a colony of 80 common marmosets (Callithrix jacchus) recently introduced to a laboratory facility. Over an 18-week period, 29 of the monkeys exhibited skin lesions that persisted for 4-6 weeks. Although eight marmosets died during the outbreak, their deaths were not attributed directly to the poxvirus infection. The skin lesions developed over the entire body surface including the soles and palms. Initially characterized as erythematous papules, they quickly changed to elevated coalescing lesions with extensive scab formation. Histopathologically, the lesions revealed moderate to marked acanthosis, and they progressed to full-thickness epidermal necrosis and ulceration. Intracytoplasmic inclusion bodies were observed occasionally within degenerate keratinocytes. These inclusions most probably constituted the intracytoplasmic aggregates of viral particles observed ultrastructurally and confirmed as members of the poxvirus group by negative staining of direct skin scrapings.     

An outbreak of Bordetella bronchiseptica pneumonia in a colony of common marmosets (Callithrix jacchus)

An outbreak of Bordetella bronchiseptica pneumonia occurred in a breeding colony of common marmosets (Callithrix jacchus). 16 animals, all except one under 12 months of age, died suddenly. Extensive lesions of pneumonia and pleurisy were found at necropsy and B. bronchiseptica was isolated from the nasopharynx, trachea and lungs. Older animals had only a mild rhinitis. Colonization of the nasal mucosa occurred in 71 of 156 marmosets.     

Exploratory behavior and learning in laboratory marmosets (Callithrix jacchus jacchus): Comparisons between experimental-cage and home-cage activity

In this paper I examine exploratory behavior and learning in two groups of common marmosets (Callithrix jacchus jacchus), both living under laboratory conditions. The main aim of my studies was to compare behavior occurring in an experimental testing situation with home-cage behavior, and to assess conditions under which exploration is enhanced. One group of marmosets was tested individually in an experimental room away from a larger animal holding room, and a second group was observed in their own home cages, surrounded by other marmosets. Marmosets in both groups were given the opportunity to learn simple tasks, such as pressing a lever for food or jumping on to a wire grid to open a door and see a neighbouring marmoset, and were provided with sets of novel or familiar objects to encourage play and exploration. In the isolated experimental cage, marmosets which learnt a lever-pressing task showed higher general activity levels than controls; in the home cages the mere addition of novel objects resulted in enhancements in exploratory behavior (measured in terms of contacts with the objects). Although the activities associated with learning tended to decline over time, the novel objects remained a constant interest throughout the experiment. The results have implications for maintaining marmosets in captivity, especially in situations when they are housed separately.     

Lymphocyte subsets in the young and aging marmoset (Callithrix jacchus)

T lymphocytes were studied in healthy young and old marmosets (Callithrix jacchus). Data indicate that monoclonal antisera to human T lymphocyte antigens can be used to identify these cells in marmosets. Total T and suppressor T cells were lower in the older group; there were no differences in helper T or in B cells. Helper/suppressor ratios (T4/T8) were increased in the older group. Thus, immune system alternations with aging and/or immune deficiency syndromes may be studied in this animal model using available reagents.     

Growth variation in common marmoset monkeys (Callithrix jacchus) fed a purified diet: relation to care-giving and weaning behaviors

Significant relations were observed between select infant-care and weaning behaviors and growth in body weight in common marmoset monkeys (Callithrix jacchus). The patterns of these relations suggest that earlier occurrence of developmental milestones, such as cessation of transport (being off carriers) and weaning to solid food, were associated with slower growth during the subsequent period. In contrast, more frequent nursing bouts during the period in which weaning was initiated were associated with higher growth rates. In the case of being off carriers, these effects did not carry over to older ages, suggesting that any deficits in growth were temporary. In the case of earlier, more frequent consumption of solid food, there was some suggestion that there were longer-term effects, followed by catch-up growth. The knee-to-heel length of subjects was not related to the measured behaviors. There was no relation between early weaning to solid food and leanness at day 75, suggesting that, although this behavior was affecting overall weight, it did not affect relative gains of fat versus lean mass. There were, however, significant correlations between cessation of transport or frequency of nursing bouts during the weaning period and leanness, with earlier cessation of transport and less frequent nursing associated with leaner infants, after weaning. Our results differed from those of a previous study that found a relation between linear growth and abuse in this species, with abuse defined as physical injury by other members of the group. We found no differences in growth between abused and nonabused infants. However, abused infants had lower birth weight.     

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.     

Sleep quantitation in common marmoset, cotton top tamarin and squirrel monkey by non-invasive actigraphy

Sleep quantitation data on the Neotropical primate species, apart from the squirrel monkey, are still sparse. As such, we have quantitated sleep in the common marmosets (Callithrix jacchus), cotton top tamarins (Saguinus oedipus) and squirrel monkeys (Saimiri sciureus) reared in one primate facility simultaneously, by non-invasive actigraphy. The range in total sleep time/24h measured for male adult common marmosets, cotton top tamarins and squirrel monkeys were 713-793 min (n=4), 707-889 min (n=4) and 459-475 min (n=2) respectively. The range in sleep episode length /12h dark phase for marmosets, tamarins and squirrel monkeys were 21-52 min (n=3), 10-28 min (n=4) and 9-15 min (n=2) respectively. Since vigilance is a critical evolutionary adaptive feature of predator avoidance among Callitrichid monkeys and squirrel monkeys, the shorter ranges in sleep episode length recorded, even under captivity, in this study could be interpreted as probable indicators of such vigilance behavior during the rest phase. We hypothesize that the vigilance behavior when it exists during a primate's active phase should also prevail when it is at rest (sleep). This hypothesis deserves additional testing in female Callitrichid monkeys.     

Changes in the size,composition, and reproductive condition of wild marmoset groups (Callithrix jacchus jacchus) in north east Brazil

Five groups ofCallithrix jacchus jacchus were studied in the field in north east Brazil. Group size and composition were similar to that described for other callitrichids, but changes in group membership occurred much more frequently than previously reported. There was a 50% turnover in group membership in a six month period, and adult males changed groups particularly often. Most groups contained only one reproductively active female, but there was evidence that one group contained two females that were reproductively active simultaneously. Some groups had several adult females, and the role of reproductive female switched from one individual to another with time. Individual marmosets are faced with an unusually wide range of alternative life history strategies involving different combinations of location and reproductive condition. We argue that marmoset social organization is best studied at the level of the whole population within an area, rather than at the level of the individual group.     

Training common marmosets (Callithrix jacchus) to cooperate during routine laboratory procedures: ease of training and time investment

The first author trained 12 laboratory-housed common marmosets (Callithrix jacchus) in pairs to assess the practicality of positive reinforcement training as a technique in the management of these nonhuman animals. Behaviors taught were (a) target training to allow in homecage weighing and (b) providing urine samples. Between 2 to 13, 10-minute training sessions established desired behaviors. Training aggressive animals only after they had been fed eliminated aggression during training. Trained animals proved extremely reliable, and data collection using trained animals was considerably faster than collection using current laboratory techniques. The results suggest that positive reinforcement training is a practical option in the management of laboratory-housed marmosets.