Social and developmental influences on urinary androgen levels in young male white-faced marmosets (Callithrix geoffroyi)

Callitrichine primates (marmosets and tamarins) often remain in their natal groups beyond the time of sexual maturity. Although studies have characterized the development of female reproductive function in callitrichine offspring, less is known about the male reproductive development. To document reproductive development in male marmosets, we monitored urinary androgen (uA) excretion in males housed in a captive colony of white-faced marmosets (Callithrix geoffroyi). Young male marmosets showed relatively low and stable rates of uA excretion early in life, with elevated production at the end of the juvenile period (9-10 months) and again at the onset of adulthood (16 months). uA levels of adult breeding males were also measured to compare to adult-aged sons. Although breeding males did have higher uA levels than their adult-aged sons, these differences did not reach conventional levels of significance. Evidence from some other reports has suggested that androgen levels of males in other species are influenced by social factors, such as the presence of a sexually receptive female or of dependent offspring. In this study, however, uA levels did not vary, based on their mothers' pregnancy status or the presence of younger siblings in the natal group. Patterns of androgen excretion in the white-faced marmoset roughly reflect those of other callitrichine species. Furthermore, unlike callitrichine daughters, gonadal activity in sons does not seem to be sensitive to within-group social cues.     

Cutting costs in response to predatory threat by Geoffroy's marmosets (Callithrix geoffroyi)

Ideally, prey should respond to their predators efficiently, without over- or underreacting to the threat. This may be particularly important for small-bodied species for whom metabolic demands are high and predatory risk is great. In the current study, two family groups of Callithrix geoffroyi living outside in a rural setting at the Center for Reproduction of Endangered Species, San Diego Wild Animal Park, were observed before, during, and after ten presentations of a great horned owl model. The owl was mounted on a post on a nearby hillside, simulating a situation in which a real but nonimminent threat is posed. As controls, a model of a crow and a cloth bag were also presented, each for ten trials. During the 10 min presentations of the owl, rates of play and foraging decreased, and rates of locomotion and vigilant looking increased from baseline rates. Data on occupation of the best viewing area suggest that the marmosets shared the job of monitoring a potential threat. After the owl was removed, behavior quickly returned to baseline rates, with the exception of looking at the place where the owl had been, and play. Neither the bag nor the crow generated significant differences from the baseline condition that preceded it. Marmosets may reduce the costs of antipredator behavior by appropriately assessing the degree of risk and by quickly resuming important activities once a potential threat has passed. Am. J. Primatol. 46:187–196, 1998. © 1998 Wiley-Liss, Inc.     

A foraging advantage for dichromatic marmosets (Callithrix geoffroyi) at low light intensity

Most New World monkey species have both dichromatic and trichromatic individuals present in the same population. The selective forces acting to maintain the variation are hotly debated and are relevant to the evolution of the ‘routine’ trichromatic colour vision found in catarrhine primates. While trichromats have a foraging advantage for red food compared with dichromats, visual tasks which dichromats perform better have received less attention. Here we examine the effects of light intensity on foraging success among marmosets. We find that dichromats outperform trichomats when foraging in shade, but not in sun. The simplest explanation is that dichromats pay more attention to achromatic cues than trichromats. However, dichromats did not show a preference for foraging in shade compared with trichromats. Our results reveal several interesting parallels with a recent study in capuchin monkeys (Cebus capucinus), and suggest that dichromat advantage for certain tasks contributes to maintenance of the colour vision polymorphism.     

Pre-retirement predator encounters alter the morning behavior of captive marmosets (Callithrix geoffroyi)

Limited data are available on the long-term effect an encounter with a predator has on its potential prey. Anecdotal reports from field research indicate that even unsuccessful attacks by predators on callitrichids have long-lasting effects. The subjects for this study were two groups of Geoffroy's marmosets (Callithrix geoffroyi) housed outside, off exhibit, at the Center for Reproduction of Endangered Species at the San Diego Wild Animal Park. Before they retired in the evening, the marmosets were observed under one of three conditions: snake model, cloth control, and no-stimulus control. Data were collected the following morning for 1 hr after the animals emerged from the sleeping box. Compared to control conditions, exposure to the snake model before retirement the previous evening was associated with significantly more vigilance checks (i.e., inspecting the area where the stimulus was last seen), and a delay in beginning to forage on the ground. These results suggest that callitrichids use recent threatening experiences to guide their vigilance behavior 12 hr after the threat is detected, and that they adjust their early morning behavior in response to potential predatory threats.     

Marmoset (Callithrix geoffroyi) Food-Associated Calls are Functionally Referential

Signals that are functionally referential provide listeners with information about a signaler's external environment, such as the presence of a nearby predator. Just as alarm calls may signal the presence of a predator, food-associated calls may signal the presence of food. To date, however, the only conclusive evidence that conspecifics perceive information about food from food-associated calls comes from a single species, the domestic chicken. Geoffroy's marmosets, small, arboreal New World primates, often emit food-associated calls when finding or consuming food. We presented playbacks of food calls and control sounds to two groups of naturalistically housed marmosets and observed the frequency of food-related behaviors (FRBs) during the 20-min post-playback period. Relative to the control playbacks, food call playbacks elicited an increase in the frequency of two FRBs (foraging and feeding), lasting throughout the post-playback observations. Moreover, the effect of food call playbacks was robust, occurring without regard to the type of food eliciting the food calls, the rate of food calling, or whether the signaler was a member of the receiver's group. To our knowledge, this research is the first to demonstrate that the food-associated calls of a primate species, like the food-associated calls of domestic chickens, meet the perception criterion for functionally referential communication. The results are discussed in light of the affective and cognitive mechanisms that may underlie the responses of receivers to hearing food-associated calls given by marmoset conspecifics.     

Demonstration of a foraging advantage for trichromatic marmosets (Callithrix geoffroyi) dependent on food colour

It has been suggested that the major advantage of trichromatic over dichromatic colour vision in primates is enhanced detection of red/yellow food items such as fruit against the dappled foliage of the forest. This hypothesis was tested by comparing the foraging ability of dichromatic and trichromatic Geoffroy's marmosets (Callithrix geoffroyi) for orange- and green-coloured cereal balls (Kix) in a naturalized captive setting. Trichromatic marmosets found a significantly greater number of orange, but not green, Kix than dichromatic marmosets when the food items were scattered on the floor of the cage (at a potential detection distance of up to 6 m from the animals). Under these conditions, trichromats but not dichromats found significantly more orange than green Kix, an effect that was also evident when separately examining the data from the end of the trials, when the least conspicuous Kix were left. In contrast, no significant differences among trichromats and dichromats were seen when the Kix were placed in trays among green wood shavings (detection distance < 0.5 m). These results support an advantage for trichromats in detecting orange-coloured food items against foliage, and also suggest that this advantage may be less important at shorter distances. If such a foraging advantage for trichromats is present in the wild it might be sufficient to maintain the colour vision polymorphism seen in the majority of New World monkeys.     

Stress reactivity in young marmosets (Callithrix geoffroyi): ontogeny, stability, and lack of concordance among co-twins

Variation in response styles in the hypothalamic-pituitary-adrenal (HPA) axis are known to be predictors of short- and long-term health outcomes. The nature of HPA responses to stressors changes with developmental stage, and some components of the stress response exhibit long-term individual consistency (i.e., are trait-like) while others are transient or variable (i.e., state-like). Here we evaluated the response of marmoset monkeys (Callithrix geoffroyi) to a standardized social stressor (social separation and exposure to a novel environment) at three different stages of development: juvenile, subadult, and young adult. We monitored levels of urinary cortisol (CORT), and derived multiple measures of HPA activity: Baseline CORT, CORT reactivity, CORT Area Under the Curve (AUC), and CORT regulation. Juvenile marmosets exhibited the most dramatic stress response, had higher AUCs, and tended to show poorer regulation. While baseline CORT and CORT regulation were not consistent within an individual across age, CORT reactivity and measures of AUC were highly correlated across time; i.e., individuals with high stress reactivity and AUC as juveniles also had high measures as subadults and adults, and vice-versa. Marmoset co-twins did not exhibit similar patterns of stress reactivity. These data suggest that regardless of the source of variation in stress response styles in marmosets, individually-distinctive patterns are established by six months of age, and persist for at least a year throughout different phases of marmoset life history.     

Hematology of common marmosets (Callithrix jacchus)

The hematology of the common marmoset (Callithrix jacchus) was investigated to provide reference values for the normal animal. Red blood cell counts, white blood cell counts, hemoglobins, mean cell volumes and differential white blood cell mean values were determined for Texas A&M colony-born animals and those obtained from the wild. The analyses were completed on 31 animals, three times each, for a total of 93 analyses, which included 16 colony-born and 15 wild-born marmosets. The hematological mean values found for marmosets were similar to those mean values reported for humans. The ranges for the hematology values were much narrower in the colony-born marmosets, and the average white blood cell count was significantly lower in these animals. This indicated that it is possible to produce and maintain a more uniform animal in the colony environment and, consequently, these animals are more suitable than wild-born animals for use as models for human research.     

Reproduction in captive common marmosets (Callithrix jacchus)

Though sexual maturation may begin at around one year of age, first successful reproduction of the common marmoset (Callithrix jacchus) is likely to be later, and it is generally recommended that animals not be mated before 1.5 years of age. The average gestation period is estimated to be 143 to 144 days. A crown-rump length measurement taken by use of ultrasonography during the linear, rapid, prenatal growth phase (between approx. days 60 and 95) can be compared against standard growth curves to estimate delivery date to within 3 to 4 days, on average. Marmosets produce more young per delivery than does any other anthropoid primate, and have more variation in litter size. Many long-established colonies report that triplets are the most common litter size, and there is documented association between higher maternal body weight and higher ovulation numbers. Higher litter sizes generally do not generate higher numbers of viable young. Marmosets are unusual among primates in having a postpartum ovulation that typically results in conception and successful delivery; reported median inter-birth intervals range from 154 to 162 days. However, pregnancy losses are quite common; one study of a large breeding colony indicated 50 percent loss between conception and term delivery. The average life span for breeding females is around six years; the range of reported average lifetime number of litters for a breeding pair is 3.45 to 4.0. Our purpose is to provide an overview of reproduction in the common marmoset, including basic reproductive life history, lactation and weaning, social housing requirements, and common problems encountered in the captive breeding of this species. A brief comparison between marmoset and tamarin reproduction also will be provided.     

Cross-fostering between two species of marmosets (Callithrix jacchus) and Callithrix penicillata)

Cross-fostering technique can be defined as adoption of infants by adults of other species. This phenomenon is poorly investigated because very young animals have few opportunities to interact peacefully with non-conspecific adults, either in captivity or in natural conditions. This study describes the induction of cross-fostering in captivity between white tufted-ear (Callithrix jacchus) and black tufted-ear marmosets (Callithrix penicillata). We conclude that this technique can be very useful for preserving the life of rejected by parents or orphan infants, mainly in the case of species with low reproduction rate in captivity or those threatened by extinction, as well for investigating the environmental effects on the typical behavior of species (courtship, food preference, vocalization patterns, e.g.).     

Respiratory disease associated with parainfluenza Type I (Sendai) virus in a colony of marmosets (Callithrix jacchus)

An outbreak of acute respiratory disease was observed in a colony of marmosets (Callithrix jacchus). Parainfluenza Type I (Sendai) virus was isolated from the lungs and from throat swabs of 2 animals which showed clinical signs of disease. A rising titre of serum neutralizing antibody to the virus isolated was detected in several affected animals. Approximately 50% of the colony showed clinical signs of disease, and 3 animals died. The duration of illness ranged from 3 to 16 days.     

Post-conflict affiliation in common marmosets (Callithrix jacchus jacchus)

Post-conflict (PC) affiliation has been demonstrated in a number of Old World monkeys and apes, but very little is known about the occurrence of the phenomenon in New World monkeys. This study examined 282 PC interactions after spontaneous conflicts around feeding time in two family groups (N = 12) of captive common marmosets, Callithrix jacchus jacchus. We found an overall corrected conciliatory tendency of 31%. Selective attraction was seen: former opponents met significantly more often in PCs than in matched controls (MCs) (27% and 16%, respectively). There was no difference in the occurrence of PC affiliation between dyads consisting of parent-offspring constellations compared to offspring-offspring constellations. PC affiliative behaviors were seen in the first three minutes following conflict termination, and consisted mainly of proximity, play invitations, and food transfer. Notably, former opponents remained within arm's reach after 17% of conflicts. Affiliation was more likely to follow after conflicts involving play issues. The functional importance of the PC affiliation in marmosets remains to be examined.     

Individual olfactory signatures in common marmosets (Callithrix jacchus)

Individual discrimination is likely a prerequisite for most primate social interactions. Olfactory cues are one set of stimuli used by primates to discriminate between individuals. Despite the importance of these olfactory signatures, there is little published research assessing the existence or function of individually unique odors among primates. This review systematically assesses behavioral and biochemical aspects of individual odors in a New World primate, the common marmoset (Callithrix jacchus). There are three objectives to this review: First, behavioral evidence for odors unique to the individual is evaluated in the context of results demonstrating that marmosets are able to discriminate between the scents from a familiar and a novel individual conspecific in behavioral bioassays under a variety of conditions. Second, biochemical evidence for individual scent signatures is debated with reference to studies examining qualitative and quantitative differences between the chemical compositions of scent-mark pools from adult females. A combined gas chromatography (GC) and mass spectrometry (MS) analysis demonstrated that each female had a unique ratio of highly volatile chemicals in the scent mark that could affect individual discrimination. Finally, the possible adaptive significance of individual odors in marmosets is debated. Individual odors may play a key role in regulating both female intrasexual competition and intersexual communication by providing a basis for the assessment of individual quality.     

Variation in steroid hormones associated with infant care behaviour and experience in male marmosets (Callithrix kuhlii)

We describe temporal patterns of change in paternal behaviour and urinary concentrations of the steroid hormones testosterone (T) and oestradiol (E(2)) in male black tufted-ear marmosets, Callithrix kuhlii, relative to the birth of their young, and test predictions of the hypotheses that (1) high levels of T are incompatible with paternal care and (2) levels of T and E(2)vary with a father's prior experience in his family group. After young were born, levels of urinary T and E(2)remained near prepartum concentrations and rates at which fathers carried infants were below peak levels until the approximate time that postpartum mating ordinarily occurs, suggesting a possible trade-off between readiness to mate and paternal behaviour in C. kuhlii. Infant-carrying behaviour of fathers occurred at its highest rate 3-4 weeks after parturition and coincided with significant declines in urinary levels of T and E(2), providing preliminary support for the hypothesis that these hormones are antagonistic to paternal behaviour. Urinary T and E(2)declined among fathers regardless of whether their young survived to weaning or died at birth, indicating that variation in these hormones after parturition occurs even in the absence of continued stimuli from infants. When adjusted for declines ordinarily associated with aging, urinary T tended to be lower among fathers with a great deal of prior experience caring for young compared with fathers having little or no experience, suggesting that either experience affects T levels of fathers, or that T levels influence fathers' chances of successfully rearing infants. Overall, our results suggest that in male C. kuhlii, T, and possibly E(2), play an important role in balancing the expression of paternal care with that of other reproductive behaviours. Copyright 2000 The Association for the Study of Animal Behaviour.     

A quantitative description of copulatory and associated behaviors of captive marmosets (Callithrix jacchus)

Measurements of male and female copulatory behavior in pairs of common marmosets were made during 30-min mating tests (n = 170). For the male,both frequencies and latencies of mounting, pelvic thrusting, and ejaculatory behaviors were analyzed. For the female, frequencies of proceptive displays (tongue-flicking) and of sexual receptivity were measured. The sexual and associated behavior of the marmoset is compared to that of other primates and the suitability of this species for laboratory studies of neurohumoral mechanisms and sexual behavior is assessed.     

Blood vitamin values of common marmosets (Callithrix jacchus)

The blood vitamin analyses of the common marmoset (Callithrix jacchus) were determined to provide baseline reference values for the normal animal. Ascorbic acid, riboflavin (erythrocyte glutathione reductase) [ECR], measurement, thiamin (erythrocyte transketolase) measurement and vitamin A (retinol) were determined for Texas A&M colony-born animals and those obtained from the wild. The analyses were completed on the animals, three times each, for a total of 93 analyses, which included 51 colony-born and 60 wild-born marmosets. A mean value of 0.98 mg/dl for ascorbic acid was found for the colony with a range from 0.06 to 4.1 mg/dl. The normal range for the marmosets appeared to be 0.5 to 1.5 mg/dl. The mean activity coefficient (AC) for the marmosets was 1.0 indicating that the animals had adequate riboflavin in the diet. The mean transketolase activities were (ribose remaining ?30.1 IU/L) and (sedoheptulose appearance ?7.9 IU/L). The mean and range for serum vitamin A (retinol) were 20.4 mg/dl and 6.96–57.44 mg/dl, respectively. None of the animals (colony-born or wild-born) exhibited any clinical signs of vitamin deficiencies as a result of being maintained in an indoor-outdoor environment over a three-year period.     

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.     

Angular momentum and arboreal stability in common marmosets (Callithrix jacchus)

Despite the importance that concepts of arboreal stability have in theories of primate locomotor evolution, we currently lack measures of balance performance during primate locomotion. We provide the first quantitative data on locomotor stability in an arboreal primate, the common marmoset (Callithrix jacchus), predicting that primates should maximize arboreal stability by minimizing side-to-side angular momentum about the support (i.e., L_sup). If net L_sup becomes excessive, the animal will be unable to arrest its angular movement and will fall. Using a novel, highly integrative experimental procedure we directly measured whole-body L_sup in two adult marmosets moving along narrow (2.5 cm diameter) and broad (5 cm diameter) poles. Marmosets showed a strong preference for asymmetrical gaits (e.g., gallops and bounds) over symmetrical gaits (e.g., walks and runs), with asymmetrical gaits representing >90% of all strides. Movement on the narrow support was associated with an increase in more “grounded” gaits (i.e., lacking an aerial phase) and a more even distribution of torque production between the fore- and hind limbs. These adjustments in gait dynamics significantly reduced net L_sup on the narrow support relative to the broad support. Despite their lack of a well-developed grasping apparatus, marmosets proved adept at producing muscular “grasping” torques about the support, particularly with the hind limbs. We contend that asymmetrical gaits permit small-bodied arboreal mammals, including primates, to expand “effective grasp” by gripping the substrate between left and right limbs of a girdle. This model of arboreal stability may hold important implications for understanding primate locomotor evolution. Am J Phys Anthropol 156:565–576, 2015. © 2014 Wiley Periodicals, Inc.