Polymorphic microsatellite loci for the common marmoset (Callithrix jacchus) designed using a cost- and time-efficient method

We describe a cost- and time-efficient method for designing new microsatellite markers in any species with substantial genomic DNA sequence data available. Using this technique, we report 14 new polymorphic dinucleotide microsatellite loci isolated from the common marmoset. The relative yield of new polymorphisms was higher with less labor than described in previous marmoset studies. Of 20 loci initially evaluated, 14 were polymorphic and amplified reliably (70% success rate). The number of alleles ranged from 3 to 9 with heterozygosity varying from 0.48 to 0.83.     

Helicobacter callitrichis sp. nov., a novel Helicobacter species isolated from the feces of the common marmoset (Callithrix jacchus)

A slowly growing microaerophilic Helicobacter species was isolated from the feces of the common marmoset (Callithrix jacchus). This bacterium possessed a pair of nonsheathed bipolar flagella, was positive for oxidase, catalase and alkaline phosphatase activities, but was negative for gamma-glutamyltranspeptidase and urease activity and for nitrate reduction. The bacterium was susceptible to nalidixic acid and resistant to cephalotine and did not hydrolyze hippurate. On the basis of phenotypic characteristics, 16S rRNA gene sequence analysis and whole-cell protein profiles, the isolate represents a new species of the genus Helicobacter, for which the name Helicobacter callitrichis sp. nov. is proposed; the type strain of the new species is R-204(T) (GenBank accession number AY192526).     

Degree of social contact affects the emission of food calls in the common marmoset (Callithrix jacchus)

The aim of this study was to investigate whether the emission of food calls in common marmosets (Callithrix jacchus) is influenced by different social contexts. Food calls are emitted by this species only in the presence of preferred food. If these calls have any communicative function, it may be that individuals produce food calls in order to call family mates toward the food source. If this is the case, the number of calls produced should vary in accordance with the number of family mates present at the moment of the discovery of the food, i.e., the fewer family mates nearby, the more food calls are emitted. This hypothesis was tested with five pairs of common marmosets, by recording the number of food calls emitted in four experimental conditions: 1). isolation: completely isolated from the family mates; 2). visual isolation: separated by a wooden panel from the family mates; 3). visual contact: separated by a wire-mesh from the family mates; and 4). physical interaction: together with the family mates. The results show that the proportion of intervals during which food calls were produced by the pairs was significantly different in the four experimental conditions. It decreased from the isolation and visual isolation condition, through the visual contact condition, reaching the lowest value in the physical interaction condition. The variation observed in the proportion of intervals during which food calls were emitted, in relation to different social contexts, is an indication in favor of the communicative function of this vocalization.     

Male parenting and response to infant stimuli in the common marmoset (Callithrix jacchus)

Callithrix jacchus infants are raised in complex family environments where most members participate in rearing the young. Many studies examining male parental behavior have focused on the carrying of infants with observations made within the family context. However, interference from family members can make it difficult to assess the father's motivation to care for infants. Our goals were to develop a testing paradigm for determining an individual's response to infant stimuli separate from family influences, compare a male's motivation to respond to an infant stimulus outside the family with his paternal behavior within the family, to compare responses to infant stimuli of parentally experienced versus inexperienced males and finally to develop a reproducible and standardized method of testing male responsiveness to infant stimulus that could serve to evaluate hormonal manipulations. Fifteen experienced common marmoset fathers were evaluated using three different measures of parental behavior: (1) instantaneous scan sampling, (2) continuous focal sampling in the family, and (3) continuous focal sampling of males presented with four infant stimuli: familiar and unfamiliar infants, familiar and unfamiliar infant vocalizations. Six parentally inexperienced males (non-fathers) served as controls. Males that carried the most in the family were typically the same males that responded most to the infant vocalization tests. Experienced fathers did not differ in their latency to enter the stimulus cage for any of the four infant stimuli response tests while inexperienced males took significantly longer to enter the stimulus cage. In addition, fathers expressed a greater frequency of infant-directed behavior than did the inexperienced males during the unfamiliar infant and unfamiliar vocalization tests. These studies show that experienced male marmosets are highly motivated to interact with infant stimuli and that there is interindividual variability in response to infant vocalizations. Testing males outside of the family allows for a clear assessment of male's interest in infant stimuli in both parentally experienced fathers and inexperienced males.     

Paracellular nutrient absorption in a gum-feeding new world primate, the common marmoset Callithrix jacchus

The common marmoset is one of the few callitrichid species that is not threatened or endangered in the wild, and is widely used in biomedical research, yet relatively little is understood about its digestive physiology. Dietary specialization on plant exudates has lead to relatively reduced small intestines, yet the common marmoset has exceptional dietary breadth, allowing it to successfully utilize a variety of habitats. We predicted that passive, paracellular nutrient absorption would be used by the common marmoset to a greater extent than in other non-flying mammals. We measured the bioavailability and rates of absorption of two metabolically inert carbohydrates not transported by mediated pathways (L-rhamnose and cellobiose, molecular masses of 164 and 342, respectively) to measure paracellular uptake, and of a non-metabolized D-glucose analog (3-O-methyl-D-glucose) to measure total uptake by both mediated and paracellular pathways. We found high bioavailability of 3-O-methyl-D-glucose (83+/-5%), and much higher bioavailability of the paracellular probes than in similarly sized non-flying mammals (30+/-3% and 19+/-2% for L-rhamnose and cellobiose, respectively). Passive, paracellular nutrient absorption accounts for around 30% of total glucose absorption in common marmosets and intestinal permeability is significantly higher than in humans, the only other species of primate measured to date. This may allow the common marmoset to maintain high digestive efficiency when feeding on higher quality foods (fruit, arthropods, gums with higher proportions of simple sugars), in spite of relatively reduced small intestines correlated with adaptations for fermentative digestion of plant gums. We find no evidence to support, in primates, the hypothesis that reliance on paracellular nutrient absorption should increase with body size in mammals, but suggest instead that it may be associated with small body size and/or taxon-specific adaptations to diet.     

The fertility of daughters in common marmoset (Callithrix jacchus jacchus) family groups

Observations previously made in the field of inter-group mating raised questions concerning the fertility of daughters in family groups and about possible competition between mothers and daughters. To test whether daughters in captive family groups could become pregnant, daughters from four groups were placed with a strange male for a period of 30 min, twice a week for eight weeks. No changes were observed in the mother/daughter interactions during the time in which the daughters were allowed contact with the strange male. Two of the daughters showed signs of ovulation and the male only copulated with these animals. One daughter became pregnant, but it was aggression with her siblings rather than her mother which necessitated removing her from her family group.     

Time course of vocal modulation during isolation in common marmosets (Callithrix jacchus)

Common marmosets vocalize phee calls as isolation calls, which seem to facilitate their reunion with family groups. To identify multiple acoustic properties with different time courses, we examined acoustic modulations of phees during different social contexts of isolation. Subject marmosets were totally isolated in one condition, were visually isolated and could exchange vocalizations in another condition, and were visually isolated and subsequently totally isolated in a third condition. We recorded 6,035 phees of 10 male–female marmoset pairs and conducted acoustic analysis. The marmosets frequently vocalized phees that were temporally elongated and louder during isolation, with varying time courses of these changes in acoustic parameters. The vocal rates and sound levels of the phees increased as soon as the marmosets saw their pair mates being taken away, and then gradually calmed down. The phee duration was longer in conditions during which there were no vocal responses from their pair mates. Louder vocalizations are conspicuous and seem to be effective for long‐distance transmission, whereas shorter call duration during vocal exchanges might avoid possible vocal overlap between mates. Am. J. Primatol. 72:681–688, 2010. © 2010 Wiley‐Liss, Inc.     

Behavioral discrimination between circumgenital odor from peri-ovulatory dominant and anovulatory female common marmosets (Callithrix jacchus)

Social peer groups of callitrichid monkeys [marmosets and tamarins] exhibit intrasexual dominance hierarchies in captivity. This laboratory study employed two-choice behavioral discrimination bioassys to test the hypothesis that scent from female common marmosets contains chemical cues that permit discrimination between dominant females in the peri-ovulatory versus luteal phase of the ovarian cycle and females holding dominant versus subordinate status. When scent from only dominant females was presented, marmosets directed significantly greater amounts of investigatory behavior toward peri-ovulatory scent versus scent collected during the luteal phase of the ovarian cycle. Animals of both sexes demonstrated significant discriminatory behavior between scent deposited by dominant versus subordinate females, but only when the dominant female was in the peri-ovulatory phase of the ovarian cycle. Test animals directed equal amounts of investigative behavior toward scent from luteal-phase dominant females and subordinate females. Female test subjects deposited significantly more scent marks over presented scents than did male subjects, particularly when the scent had been donated by a peri-ovulatory female. Chemical odors specific to the peri-ovulatory and luteal phases of the ovarian cycle may play a role in mediating behavioral interactions among marmosets. Am. J. Primatol. 46:265–284, 1998. © 1998 Wiley-Liss, Inc.     

Radiographic Evaluation of Appendicular Skeletal Maturation in the Common Marmoset (Callithrix jacchus)

The thoracic appendicular skeletal development of five common marmosets was monitored radiographically at weekly intervals from 1 day to 94 weeks of age and the times of appearance and fusion of 47 ossification centers were recorded. A range and average age for the appearance and fusion of each ossification center were calculated and compared to data available for the rhesus monkey and man.     

Responses to natural and synthetic phee calls by common marmosets (Callithrix jacchus)

Captive adult common marmosets (Callithrix jacchus) produce whistlelike “phee” calls in two contexts: in the home cage, where phee calls may function as part of territorial marking behavior, and when separated from social companions, where phee calls may function to reunite conspecifics. Natural and synthesized calls representing the acoustic structure of male and female calls in each context were presented to adult marmosets in a playback paradigm. Marmosets demonstrated discriminative abilities according to the context of the call and the caller's sex. Vocal and behavioral responses indicated increased vigilance and territorial behavior, following playbacks of naturally produced calls as well as synthetic calls. All animals scanned more frequently following produced calls as well as synthetic calls. All animals scanned more frequently following natural home cage as well as isolation calls, but only increased contact behavior (trills) in response to home cage calls. The responses were dimorphic according to the sex of the caller, where adult males scanned more following male calls, and adult females were more aggressive following male and female calls. The differential behavioral responses to playbacks of marmoset phee calls suggest a biological relevance to subtle differences found in the acoustic parameters of the phee call. © 1994 Wiley-Liss, Inc.

1 This article is a US Government work and, as such, in the public domain in the United States of America.

     

An experimental analysis of social interaction in the common marmoset (Callithrix jacchus jacchus)

Adult and juvenile common marmosets were introduced to unfamiliar conspecifics individually and in whole groups. In introductions using animals of the same sex, adults were mutually hostile unless they were related or socially familiar; juveniles behaved submissively to adults and little aggression was observed between juveniles. In introductions using animals of the opposite sex, males of all ages solicited females but females did not reciprocate. When whole groups were introduced, in two experiments most of the elder group members behaved aggressively and younger animals did not interact frequently; but in a third experiment, in which the adult males were related, little aggression was observed and younger animals behaved amicably. It is argued that the behavioral reactions shown by individual marmosets are related to territorial hostility and that the behavior of juveniles to adults may aid assimilation of younger animals into new groups.     

Alloparental Responsiveness to Newborns by Nonreproductive,Adult Male,Common Marmosets (Callithrix jacchus)

Parental care in mammals is influenced by sensory stimuli from infants, and by changes in the hormone levels of caretakers. To determine the responsiveness to infant cues in nonreproductive adult male common marmosets (Callithrix jacchus) with and without previous experience in caretaking, we exposed 12 males to newborn marmosets and assessed their cortisol plasma levels and behavioral response. Newborn marmosets housed in transparent enclosures were placed inside the cages of the adult male subjects. Males were exposed four times to two different experimental conditions: (a) newborn enclosures remained closed during the observation period and (b) newborn enclosures were opened during the observation period to allow direct social interaction by the adult males. Blood samples from adult males were collected after each behavioral observation trial to measure the levels of cortisol. The behavioral responses of adult males exposed to the closed and open newborn enclosures showed a significant difference only with respect to the frequency of displacements, where males moved among the quadrants of their own cages with greater frequency when the newborn enclosure was sealed. Experienced males approached newborn enclosures more frequently, spent more time in close proximity, and carried and recovered newborns more quickly than inexperienced males. The successive exposure to newborns increased the responsiveness in inexperienced males. The highest levels of plasma cortisol in adult males were recorded following periods of exposure to the sealed newborn enclosures. This suggests that successive exposure to newborns and previous alloparental caregiving experience while living in family groups influences the responsiveness of male marmosets to the sensory cues of newborns. Am. J. Primatol. 75:145‐152, 2013. © 2012 Wiley Periodicals, Inc.     

A case report of spontaneous opening of congenitally fused labia in a female common marmoset (Callithrix jacchus) followed by pregnancy and birth of twins

A first case of spontaneous opening of congenitally fused labia (CFL phenotype) in a captive common marmoset followed by pregnancy and birth is presented here. The occurrence of this phenotype has been previously published in captive marmosets, but so far the etiology is unknown.     

Social context affects phee call production by nonreproductive common marmosets (Callithrix jacchus)

Common marmosets produce two variants of their long call (phee call) in different situations. Intergroup calls are produced in territorial situations, and intragroup separation calls are produced by marmosets isolated from group members. Marmoset groups frequently include postpubertal, nonreproductive members; their roles in the spontaneous production of territorial vocalizations is unclear. This study analyzed the production of home cage phee calls by nonreproductive, postpubertal marmosets while they were housed in their natal groups and after pairing with an opposite-sex conspecific. Additionally, the production of the separation phee call variant was assessed in both social conditions. The results indicated that the marmosets rarely produced home cage, or territorial, phee calls while they were natally housed. In contrast, both males and females produced the territorial phee call at a much higher rate as early as 4 days after pairing. Age-matched females remaining in their natal groups throughout the study produced home cage phee calls infrequently. Most marmosets produced separation phee calls at a high rate after separation from either their natal group or a partner, suggesting that the makeup of a social group has little effect on an animal's motivation to reunite with conspecifics. These results suggest that the social environment has an important influence on the production of territorial phee calls. Am. J. Primatol. 43:135–146, 1997. © 1997 Wiley-Liss, Inc.     

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.     

Congenitally caused fused labia in the common marmoset (Callithrix jacchus)

In this paper, the occurrence of an external genital abnormality in female marmoset monkeys (fused labia) is discussed. This malformation was detected, for the first time, in a group of animals at the German Primate Center (GPC), Goettingen. The malformed vulva was completely sealed except for an opening of 1.5-2.5 mm around the urethra sufficient for urination. Because of this defect the animals were not able to copulate. As a consequence, the affected females were functionally infertile although they had a normal genital tract and a regular cycle. This vulvar abnormality was found in 12 females, offspring of 10 pairs in which either one or both came to the German Primate Center from two genetically related colonies in Munich, Germany, and one colony in Basel, Switzerland. The abnormality appeared to be recessive and inheritable from either parent. In pairs in which both animals were from one of the mentioned colonies, 45% of the female offspring were affected. In pairs where only one partner came from these colonies, 26% of female offspring had the malformation. These results indicate that avoidance of inbreeding, which is frequently performed in primate colonies, may reduce, but not eliminate the expression of abnormalities of genetic origin. Therefore selective breeding is required, and, in colonies where these recessive mutations are widespread, the development of genetic screening tests would be advantageous.     

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.