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.     

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.     

Evaluation of vitamin D3 metabolites in Callithrix jacchus (common marmoset)

Vitamin D₃ (cholecalciferol) is endogenously produced in the skin of primates when exposed to the appropriate wavelengths of ultraviolet light (UV-B). Common marmosets (Callithrix jacchus) maintained indoors require dietary provision of vitamin D₃ due to lack of sunlight exposure. The minimum dietary vitamin D₃ requirement and the maximum amount of vitamin D₃ that can be metabolized by marmosets is unknown. Observations of metabolic bone disease and gastrointestinal malabsorption have led to wide variation in dietary vitamin D₃ provision amongst research institutions, with resulting variation in circulating 25-hydroxyvitamin D₃ (25(OH)D₃), the accepted marker for vitamin D sufficiency/deficiency. Multiple studies have reported serum 25(OH)D₃ in captive marmosets, but 25(OH)D₃ is not the final product of vitamin D₃ metabolism. In addition to serum 25(OH)D_3, we measured the most physiologically active metabolite, 1,25-dihydroxyvitamin D₃ (1,25(OH)₂D₃), and the less well understood metabolite, 24,25-dihydroxyvitamin D₃ (24,25(OH)₂D₃) to characterize the marmoset's ability to metabolize dietary vitamin D₃. We present vitamin D₃ metabolite and related serum chemistry value colony reference ranges in marmosets provided diets with 26,367 (Colony A, N = 113) or 8,888 (Colony B, N = 52) international units (IU) of dietary vitamin D₃ per kilogram of dry matter. Colony A marmosets had higher serum 25(OH)D₃ (426 ng/ml [SD 200] vs. 215 ng/ml [SD 113]) and 24,25(OH)₂D₃ (53 ng/ml [SD 35] vs. 7 ng/ml [SD 5]). There was no difference in serum 1,25(OH)₂D₃ between the colonies. Serum 1,25(OH)₂D₃ increased and 25(OH)D₃ decreased with age, but the effect was weak. Marmosets tightly regulate metabolism of dietary vitamin D₃ into the active metabolite 1,25(OH)₂D₃; excess 25(OH)D₃ is metabolized into 24,25(OH)₂D₃. This ability explains the tolerance of high levels of dietary vitamin D₃ by marmosets, however, our data suggest that these high dietary levels are not required.     

Diurnal variation on the excretion patterns of fecal steroids in common marmoset (Callithrix jacchus) females

The use of fecal steroid analysis to assess gonadal and adrenal function in primates has rapidly increased in recent years due to the ability to collect feces from nonhuman primates living in wild conditions. These techniques offer an exciting new potential for enhancing our knowledge of the endocrine status of free-living animals. Prior to using these techniques under field conditions, it is important to determine the diurnal variation of fecal excreted steroids for assessing possible time limitations on fecal collections. The following study investigates the diurnal frequency of defecation and patterns of steroid levels excreted in feces from four female common marmosets, Callithrix jacchus, living in a family group. These females represented three reproductive conditions: early pregnancy, ovarian cycling, and noncycling (postpubertal). Cortisol, estradiol, and progesterone were extracted and analyzed by enzyme immunoassay. Diurnal variations in steroid levels were found by ANOVA for cortisol and progesterone but not for estradiol. Significantly higher levels of cortisol were found in the afternoon, while the reverse was found for progesterone. All females showed the same pattern of steroid level change, except for cortisol in the pregnant female. Since all females defecated within the first hour after they awoke in the morning, this time was determined to be the most effective time to collect feces. The consistency of our findings reinforces the usefulness of this approach for studying reproductive and adrenocortical function in marmosets and also indicates that fecal collection should be limited to either morning or afternoon collections. Am. J. Primatol. 46:105–117, 1998. © 1998 Wiley-Liss, Inc.     

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.     

Urine collection in the common marmoset (Callithrix jacchus) and its applicability to endocrinological studies

We investigated a new method of urine collection in the common marmoset. We entered the cage as soon as the light cycle started in the breeding room and collected urine from the animal directly without any restraint. We were able to take separate samples from completely different individuals housed together for behavioral studies in the same cage. Urine and blood samples were taken from individuals from late pregnancy through postpartum nursing period. Cortisol and prolactin concentrations measured in urine were compared to those measured in blood to evaluate this collection method. LH/CG level in the urine samples was also measured. Urine data in females indicated a tendency toward high cortisol values during late pregnancy, a sharp drop before parturition, and increase after delivery. In females cortisol levels measured in blood closely resembled concentrations measured in urine. Urine cortisol in males clearly indicated an increase postpartum, but the increase was not indicated in plasma. Plasma and urine prolactin concentrations in females made a similar increase during lactation. Male's plasma prolactin clearly indicated an increase directly proportional to strong behavioral contact with the infant. We also confirmed hormonal changes during pregnancy, and postpartum ovulation and subsequent pregnancies, from urine LH/CG data. We found this method extremely useful because of the high correlation between cortisol, prolactin and LH/CG data from blood and urine. Additionally, we collected urine samples with little stress to the animal from fear, irritation, pain, etc.     

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.     

Molecular cloning and functional characterization of endogenous recombinant common marmoset monkey (Callithrix jacchus) follicle-stimulating hormone

Background Common marmoset monkeys (Callithrix jacchus) are readily used in biomedical research. However, superovulation for embryonic stem cell production and developmental research still remain difficult. Inexplicably, follicle‐stimulating hormone (FSH) as key player in superovulation has to be administered in extremely high dosages in this non‐human primate compared to human. Methods To evaluate whether marmoset FSH (cjFSH) is functionally more competent than its human homologue on the marmoset FSH receptor (cjFSHR), we established in vitro a homologous system characterizing homologous and recombinantly produced cjFSH. Results Upon stimulation of two cell lines stably expressing either the marmoset or the human FSH receptor (cj/hFSHR), respectively, the second messenger signaling of the activated receptor displayed no significant difference in ED₅₀ values. Thermostability of cjFSH was significantly prolonged by roughly 20% on both FSHRs. Conclusion High FSH dosage in marmoset superovulation cannot be explained by enhanced biopotency of the natural animal’s gonadotropin.     

Handedness in the common marmoset (Callithrix jacchus)

For about 20 months the development of hand preferences in 21 experimentally naive common marmosets (Callithrix jacchus) was examined in 15 different tests. Test preferences were compared with their spontaneous behavior preferences in such contexts as feeding, grooming, play, and others. In the spontaneous use of the hands, only eight animals showed a significant lateral preference (2 left-handed, 6 right-handed). During the test period, however, the number of handed marmosets increased to 19 (5 left-handed, 14 right-handed). Most of the animals fluctuated considerably in their preference levels, a situation which led to a remarkable test response inconsistency of handedness. When the test situation was changed, complete reversals of handedness were more frequent than weakening or strengthening of a particular preference. The animals' emotions during the test session and environmental variables affected handedness significantly. None of the tested marmosets showed an increase of hand preference from the first to the last test. Our results indicate that Callithrix is ambidextrous rather than handed.     

Circadian pattern of plasma melatonin concentrations in the marmoset monkey (Callithrix jacchus)

This study describes the concentrations of melatonin in plasma samples taken from marmoset monkeys (Callithrix jacchus) every 4 h over three 24-h periods. A circadian pattern of secretion was apparent, with higher levels recorded at night (20.00–08.00 h) than during the day (08.00–20.00 h) and a peak concentration at 20.00 h. There was a significant difference in the mean day and night concentrations (32.5 ± 4.5 pg/ml versus 49.0 ± 6.9 pg/ml, respectively) with individual concentrations ranging between<10–60 pg/ml in the day and 15–200 pg/ml at night. Circadian plasma melatonin concentrations were similar over the three 24-h periods, in male (n = 3) and female (n = 3) monkeys, and in dominant (cyclic, n = 5) and subordinate (acyclic, n = 4) females. The results show a less pronounced circadian profile in the marmoset than is seen in the human but a similar profile to that in the seasonally breeding rhesus monkey.     

Minimally invasive transabdominal collection of preimplantation embryos from the common marmoset monkey (Callithrix jacchus)

A novel, minimally invasive, transabdominal embryo collection method (transabdominal method) was developed as an alternative to a standard abdominal incision for embryo collection in the common marmoset. The abdominal incision method was used for 304 flushes using 36 female animals, whereas the transabdominal method was used for 488 flushes using 48 females; successful embryo collection rates were 48.0% and 48.4% (P > 0.05), respectively. These techniques were successfully duplicated at another institute (German Primate Center, DPZ). At that institution, successful embryo collection rates were 88.9% and 77.8% for the abdominal incision and transabdominal methods, respectively (P > 0.05), whereas the average numbers of preimplantation embryos obtained per flush were (mean ± SD) 1.91 ± 0.35 and 1.71 ± 0.14 (P > 0.05). The transabdominal method reduced animal stress, did not require incisional wound healing, and enabled successive embryo recoveries to be done much sooner. More embryos in early developmental stages (zygotes/morulae) were recovered using the transabdominal method (76.1%) than the abdominal incision method (52.6%, P < 0.01). In contrast, recovery of arrested or abnormal embryos was not significantly different between these two methods (9.8% and 8.3%). To verify developmental ability of embryos recovered by the transabdominal method, transfer of 28 normal embryos to 14 surrogate mothers yielded a nidation rate of 57%. Five females sustained term pregnancies and eight neonates were born. This novel transabdominal method will facilitate progress in marmoset developmental biology and embryology.     

Pregnancy diagnosis in the common marmoset (Callithrix jacchus jacchus).

Abdominal palpation of the uterus was carried out on 25 pregnant and 29 non-pregnant marmosets (Callithrix jacchus jacchus). 195 complete 24-hour urine specimens, collected between the first week of gestation and term (21 weeks), were tested with the Sub-Human Primate Tube (SHPT) test. No significant differences between the two methods in their ability to diagnose pregnancy were obtained between the first and 13th week of gestation. The SHPT test was seldom positive after the 13th week of pregnancy, whereas, with one exception, palpation always indicated pregnancy.     

Intragroup agonistic behavior in captive groups of the common marmosetCallithrix jacchus jacchus

Agonistic behavior was observed in five captive groups of the monogamous monkey Callithrix jacchus jacchus,which normally produces twin offspring every 5 months. Fighting is first recorded when twins are aged 5–10 months. These “twin fights” determine differences in status between combatants that can be detected 5 months later. From what is known of the social behavior of the species, it is postulated that an individual’s twin is its most serious rival and that early fighting is advantageous because injury is minimal while the animal retains its milk dentition. In contrast to twin fights, aggression between same-sex juveniles and adults does not involve long fights and probably serves to reinforce preexisting differences in status. It often results in forcing a group member to the periphery, and therefore, its main function may be to drive mature, same-sexed individuals out of the group. Apart from the relationship between twins, status within the family group is age related and not normally determined by aggression.     

Intestinal cryptococcosis in a common marmoset (Callithrix jacchus)

A five-year-old female common marmoset (Callithrix jacchus) died after a one-month clinical course of nonspecific signs. Pathologic findings were acute diffuse fibrinonecrotizing enteritis and granulomatous endolymphangitis of intestinal and mesenteric lymphatic vessels. Both lesions were associated with a marked proliferation of Mayer's mucicarmine-positive, 4 to 15 microm yeasts that were surrounded by a wide clear halo. The infection was probably acquired by oral route. Other findings included moderate multifocal granulomatous and necrotizing hepatitis and mesangial nephropathy. Although the immunological status of this marmoset was unknown, cryptococcosis might induce primary lethal intestinal infections in callitrichids.     

Serum levels of prolactin during the ovarian cycle,pregnancy, and lactation in the common marmoset (Callithrix jacchus)

A homologous double-antibody radioimmunoassay developed for humans was used to measure serum prolactin, progesterone, and estradiol in common marmosets. In the ovarian cycle of common marmosets, serum progesterone began to increase after an estradiol surge, attained a peak level, and then declined before the ensuing pre-ovulatory rise in estradiol. During the luteal phase, the change in serum concentrations of estradiol was synchronized with that of progesterone. During the ovarian cycle there was no consistent change in serum prolactin concentrations. During the last 75 days of pregnancy the prolactin level was higher than during the ovarian cycle and the first 70 days of pregnancy. Moreover, during lactation, mothers with suckling twin infants had a higher prolactin level than during the final stage of pregnancy.     

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).     

Early learning in the common marmoset (Callithrix jacchus): Behavior in the family group is related to preadolescent cognitive performance

Early environment can have a major impact on development, with family life known to play an important role. Longitudinal studies can therefore help increase our understanding of variance in cognitive abilities in young animals, as well as over time. We followed 22 marmosets (11 male and 11 female) from infancy through to early adolescence. At 3 months old, the marmosets were trained to reliably touch a rewarded stimulus. At 5 months, behavior was observed within the natal group. At 9 months, the marmosets were given a visual discrimination task to assess learning ability. Mann–Whitney U tests found no sex or family size differences in number of errors at 3 or 9 months. While no significant relationships were found between behavior in the family and learning at 3 months, significant negative correlations were found between duration spent in locomotion and learning errors (p = .05), as well as between frequency of calm vocalizations and learning errors (p = .001) at 9 months. A U-shape curve was found between amount of social play and learning at 9 months. Positive family interactions, including moderate amounts of play, as well as calm individual behavior, may therefore be important in learning. This study sheds light on cognitive development in much younger marmosets than previously studied, and helps increase understanding of how individual differences in learning may arise.