Captive Marmosets Research Articles

The Development of Obesity Begins at an Early Age in Captive Common Marmosets (Callithrix jacchus)

Animal models to study the causes and consequences of obesity during infancy in humans would be valuable. In this study, we examine the patterns of fat mass gain from birth to 12 months in common marmosets (Callithrix jacchus). Lean and fat mass was measured by quantitative magnetic resonance at 1, 2, 6, and 12 months for 31 marmosets, 15 considered Normal and 16 considered Fat (> 14% body fat) at 12 months. Animals were fed either the regular colony diet mix or a high-fat variation. Subjects classified as Fat at 12 months already had greater lean mass (198.4 +/- 6.2 g vs. 174.0 +/- 6.8 g, P = 0.013) and fat mass (45.5 +/- 5.0 g vs. 24.9 +/- 3.4 g, P = .002) by 6 months. Body mass did not differ between groups prior to 6 months, however, by 1 month, Fat infants had greater percent body fat. Percent body fat decreased between 1 and 12 months in Normal subjects; in Fat subjects, it increased. The high-fat diet was associated with body fat > 14% at 6 months (P = 0.049), but not at 12 months. This shift was due to three subjects on the normal diet changing from Normal to Fat between 6 and 12 months. Although maternal prepregnancy adiposity did not differ, overall, between Normal and Fat subjects, the subjects Normal at 6 and Fat at 12 months all had Fat mothers. Therefore, diet and maternal obesity appear to have potentially independent effects that may also vary with developmental age. Although birth weight did not differ between groups, it was associated with fat mass gain from 1 to 6 months in animals with > 14% body fat at 6 months of age (r = 0.612, P = 0.026); but not in 6-month-old animals with < 14% body fat (r = -0.012, P = 0.964). Excess adiposity in captive marmosets develops by 1 month. Birth weight is associated with adiposity in animals vulnerable to obesity.

Olfactory Cues Modify and Enhance Responses to Visual Cues in the Common Marmoset (Callithrix jacchus)

Diurnal primates are generally considered to have a poor sense of smell and a dearth of publications in primate olfaction has done little to correct this view. We know, however, that New World monkeys, such as the common marmoset (Callithrix jacchus), have a well-developed olfactory system and display olfaction-based social behaviour. We have far less certainty as to the role of olfaction in predator- and food- based odours in Callithrichids, and indeed, in many other primate species. We also know very little about the relative importance of multi-modal cues (such as visual and olfactory stimuli combined). If visual perception is dominant, one would expect that adding perceptual cues in other modalities would elicit no or only insignificant changes in behaviour. If, however, olfaction has a greater role to play in foraging, predator detection and anti-predator responses, experimental investigations should be able to confirm this readily. We therefore tested how a colony of captive marmosets responded to a range of predator- and food-based odours and how the presence of a specific odour was expressed in behavioural changes. We found that the predator-naive marmosets responded strongly against faecal odours of predators (withdrawal) and with considerable curiosity (attraction) to favourite food-based odours. Signs of fear and pleasure were also noted. We then combined the most unpleasant and pleasant odours with the corresponding visual stimuli to test whether the addition of olfactory cues changed behaviour in comparison with that shown for visual stimuli alone. We found that there was a reduced latency to approach a food item when its odour was detectable and that vigilance increased markedly when a predator could be smelt as well as seen. These results suggest that marmosets perceive and respond to specific olfactory information and that olfaction may be more important for a broad range of functions not previously considered.

Influence of Different Light Intensities on the Daily Grooming Distribution of Common Marmosets Callithrix jacchus

The daily distribution of autogrooming was evaluated in adult marmosets submitted to different illumination intensities in the light phase of the light-dark cycle. Autogrooming and locomotor activity were monitored and the faecal cortisol level assessed as a stress indicator. The distribution of autogrooming showed two distinct tendencies: when the light intensity varied from 500 to 200 lux, a slight increase in frequency and duration was observed, while a significant decrease in both variables occurred at 10 lux. Varying light intensities did not inhibit rhythm synchronization. The daily profile of autogrooming was mainly unimodal with an acrophase in the first half of the light phase. Faecal cortisol levels tended to increase in animals submitted to 100 and 10 lux, but these results are not conclusive. We suggest keeping captive marmosets in light intensities of at least 200 lux in the light phase, allowing animals to maintain autogrooming levels in order to reduce the discomfort caused by captivity and isolation.

Risco de transmissão do vírus da raiva oriundo de sagui (Callithrix jacchus), domiciliado e semidomiciliado, para o homem na região metropolitana de Fortaleza, estado do Ceará

In the State of Ceará, a new variant of the rabies virus was identified associated with cases of human rabies transmitted by common marmosets (Callithrix jacchus), which are frequently kept as pets. This new variant does not present antigenic proximity or genetic relationship to variants of the virus isolated from bats and terrestrial mammals from the American continent. The present study aimed to evaluate the risk factors of rabies virus transmission from common marmosets (C. jacchus) maintained as pets in the metropolitan region of Fortaleza, State of Ceará, Brazil, to human beings. A questionnaire focusing on animal management and interaction between humans and primates was applied to individuals who had marmosets in the municipalities of Aquiraz and Maranguape. In order to evaluate the presence of rabies antigens by direct immunofluorescence test (DIF), samples of saliva were collected from domiciliary captive marmosets. Based on the detection of rabies antigens, biopsy samples of central nervous system (CNS) were analyzed. Analysis of questionnaire data verified that a close relation exists between humans and their pet marmosets, especially during management practices. Additionally, these people showed minimal knowledge regarding rabies, which represents a greater risk of infection. Of the 29 saliva samples evaluated, one (3.4%) was positive for DIF reaction and of the 11 CNS samples, three (27.3%) were positive. Laboratory data are in agreement with the questionnaire findings, which confirm an increased risk of rabies virus transmission due to the close relation between humans and marmosets.

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.

Some aspects of sexuality and reproduction in groups of captive marmosets (Callitbrix jacchus).

Several aspects of sexual and reproductive behaviour of Callithrix jacchus were studied for almost five years. The most important results are as follows: (1) In artificial groups (AG), heterosexual interactions were observed with varying frequencies between all group members; in the family groups (FG), however only between the parents (a-male and a-female). (2) In general, sexual interactions between two animals in the AG were tolerated by the other group members; in the FG, the offspring tried to disturb all copulations between the parents. (3) Pre- and postcopulatory play, and copulation with intromission and ejaculation are limited to the highest ranking group members. No difference was found between the highest and lower ranking males in the duration of copulation and number of pelvic thrusts. (4) The breeding privilege is correlated with rankorder; that is, only the most dominant male and female reproduce. This gives the impression of a monogamous relationship between the a-animals. (5) Independent of follicle maturation and ovulation, the a-females indicate estrous characterized by a considerable increase in willingness to copulate, associative behaviour between the a-male and the a-female (both most likely influenced or caused by pheromone activity), as well as aggressive behaviour between the a-female and the lower ranking females in the AG. Conflicts between the dominant and lower ranking group members, especially the females in AG, usually cause the group to split. The ability of the lower ranking females to reproduce is adversely affected by the stress to which they are subjected. (6) The parents of the FG are extremely tolerant of their sexually mature adult sons and daughters; expulsion of offspringe by the parents has not occurred as yet in the FG. (7) There is no certain evidence of cyclic visible changes of the genital region or menstrual bleeding in C. jacchus. (8) Captive C. jacchus females breed all year long; gestation is 144--146 days. (9) Homo- and autosexuality is reported for the males of the FG.

Effect of Nest Box Availability on the Circadian Activity Rhythm of Common Marmosets (Callithrix jacchus)

The effect of nest box availability on the circadian activity rhythm (CAR) was compared in a diurnal primate kept in two conditions: with and without nest box, in a light-dark (LD) cycle (12:12) and constant light (LL). Marmosets kept in LD without nest box showed a longer duration of the activity phase (α), smaller day-to-day variability in activity onset and offset and higher levels of activity, particularly towards the end of the activity time. In LL, all animals maintained with nest box expressed free-running CAR, but without nest box, 3 of the 4 individuals showed relative coordination with the outdoor LD cycle, possibly due to social synchronization with captive marmosets maintained outdoors. All animals showed longer α and higher levels of activity without nest box. Thus, the availability of a nest box is an important aspect in maintaining marmosets, influencing CAR expression in this diurnal primate in LD and LL conditions, possibly due to differences in light exposure that induces masking. Further studies are needed to evaluate the effects of the unavailability of a nest box on CAR in LL conditions.

Changes in experimental conditions alter anti-predator vigilance and sequence predictability in captive marmosets

Anti-predator vigilance and its sequence predictability in captive adult male black tufted-ear marmosets (Callithrix penicillata) was analyzed under three experimental conditions: (1) four novel (maze) environment habituation trials; (2) six taxidermized (cat) predator confrontation trials in the same maze environment; and (3) four additional maze-only trials, in the absence of the cat stimulus. Significant quantitative and qualitative differences (aerial vs. terrestrial) were observed in scan and glance behaviors within and between the three experimental conditions. Furthermore, inter-scan bout sequence significantly deviated from randomness during the initial maze habituation and predator confrontation trials, as well as during all predator removal trials. This parameter, however, followed a random pattern during the course of the remaining sessions. Therefore, vigilance in marmosets seems to be an important and highly organized component of this species' anti-predation repertoire, inasmuch as it occurs at high rates, alters according to specific environmental cues and has a subtle differential adaptive response after repeated trials.

The composition of milk from free‐living common marmosets (Callithrix jacchus) in Brazil

Common marmosets, one of the smallest anthropoid primates, have a relatively high reproductive rate, capable of producing twins or triplets twice per year. Growth and development of infants is relatively rapid, and lactation is relatively short at less than 3 months. Although mean values for the proximate composition (dry matter, protein, fat and sugar) of captive common marmoset milks fall within anthropoid norms, composition is highly variable among individual samples, with concentrations of milk fat ranging from below 1 to over 10%. To examine the extent to which this variation might be a consequence of captive conditions, we collected milk samples from wild common marmosets freely living on a farm in the state of Rio de Janeiro, Brazil. The proximate composition of the milk samples was assayed using identical techniques as used for the captive marmoset milks. The composition of the milk of wild common marmosets was also variable, but tended to be lower in dry matter, fat, protein and gross energy, and higher in sugar than milks from captive animals. Interestingly, the percentage of estimated gross energy from the protein fraction of the milks was relatively constant in both wild and captive marmosets and did not differ between wild and captive animals: 1 kcal of common marmoset milk contains on average (+/-SEM) 0.035+/-.001 g of protein regardless of the gross energy content of the milk or whether the milk was from a wild or captive animal. In contrast, in 1 kcal of low-energy milks, the amount of sugar was significantly higher and the amount of fat significantly lower than in 1 kcal of high-energy milks. Thus, common marmoset milk exhibits axes of variability (especially fat concentration) as well as a significant stability in the relative amount of protein.

Food distribution effects on the behaviour of captive common marmosets,Callithrix jacchus

AbstractCommon marmosets,Callithrix jacchus, are widely used by research laboratories and are commonly provided with food in bowls. These centralised, unchallenging sources of food result in high foraging success for low foraging effort. Foraging devices, which require more skill and effort for foraging success, may broaden the behavioural profiles of marmosets by including more elements of their natural ethogram, reflecting improved welfare. The behaviour of eight female common marmosets was examined as a function of four different food distributions: food centrally located in a stationary bowl; food in a bowl that changed location each day; food centrally located in a stationary bowl, in addition to hidden food in a clustered food source (cluster feeder) or hidden food in dispersed food sources (dispersed feeders). Both the cluster and dispersed feeder distributions increased foraging, and there was a trend for reduced scratching and grooming in the presence of the feeders compared with the bowl-only treatments. The cluster feeder increased the amount of time a marmoset spent in a large room annexed to the home rooms more than the dispersed feeders, and this effect was sustained throughout the day after the feeders had been removed. Both feeders increased activity and movements within all areas of the annexed room compared with the bowl-only treatments; therefore, both feeder types improved the welfare of the captive marmosets more than the provision of food bowls.

Rapid habituation of scan behavior in captive marmosets following brief predator encounters

Scan behavior in 10 captive predator-naive adult black tufted-ear marmosets (Callithrix penicillata) was investigated prior, during and following brief predator encounters (taxidermized oncilla cat -- Leopardus tigrinus) versus neutral stimulus exposures (stuffed toy). For each stimulus, three 9 min home-cage trials were conducted > or = 72 h apart. Each trial was divided into three consecutive 3 min intervals: pre-exposure baseline observation, stimulus exposure, and post-exposure observation period. Post-exposure scan duration increased during the first two predator confrontations, while scan frequency increased significantly only after the first. Scan behavior remained constant within the last predator encounter, as it also did within and between the three neutral stimulus exposures. Although marmosets scanned more often and significantly longer after encountering the predator than the neutral stimulus, this response rapidly habituated by the second trial. Therefore, black tufted-ear marmosets in a familiar environment rapidly habituate to brief repeated predator encounters, possibly minimizing anti-predation costs once the degree of a potential threat has been adequately assessed.

Mobbing vocalizations as a coping response in the common marmoset

Using a non-invasive method of sampling saliva followed by assay for cortisol levels, we found that common marmosets ( Callithrix jacchus) show a decrease in cortisol levels after seeing a snake-model stimulus that reliably elicits mobbing (tsik) calls. In fact, there was a significant positive correlation between the number of tsik vocalizations made and the magnitude of the decrease in the cortisol concentrations. Furthermore, marmosets with higher levels of cortisol prior to being exposed to the stimulus produce more tsik calls than those with lower levels of cortisol. Subsequent experiments showed that, in response to 15 min of isolation with no visual or auditory contact with conspecifics (a traditional stressor), cortisol levels increased significantly. However, playback of the mobbing calls of a familiar conspecific to individual isolated marmosets not only prevented the rise in cortisol, but also actually caused a decrease in the levels of this hormone. This suggests that the mobbing calls serve to calm the marmoset after experiencing a stressful situation. This finding results in a greater understanding as to the role of physiological responses during communication in this species and could have implications for the welfare of marmosets in captivity.

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

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

Analysis of infant carrying in large, well-established family groups of captive marmosets (Callithrix jacchus)

To assess the pattern of infant carrying across time and family members, we counted which animals in 13 well-established family groups of captive-bred marmosets (Callithrix jacchus) carried neonates during the first 8 weeks of life. The neonates were carried almost continuously for the first 3 weeks and then spent progressively more time independently. The mother did most of the carrying for the first 2 weeks, her contribution rising from day 1 to day 3 and declining thereafter. The contribution of the father was high on day 1, declined during the first week, and then rose to a peak in the fourth week. The contribution of the siblings rose sharply during the first week and declined thereafter. There was no overall difference in amount of infant carrying by each parent. The contribution of each sibling was small although in these large families the total contribution by siblings was large. These data may differ from previous observations because the breeding pairs were very well established, the families were large, and all except the youngest animals were very experienced in rearing and carrying. These data emphasise the group-dynamic nature of infant carrying in a primate species.

Actinobacillus actinomycetemcomitans genetic heterogeneity: amplification of JP2-like ltx promoter pattern correlated with specific arbitrarily primed polymerase chain reaction (AP-PCR) genotypes from human but not marmoset Brazilian isolates.

Specific clonal types of Actinobacillus actinomycetemcomitans, a major human periodontal pathogen, may be responsible for clinical manifestations and the production of leukotoxin virulence factors. Leukotoxicity is associated with genetic polymorphism at the promoter region of the leukotoxin (lItx) gene. Here, we describe the use of arbitrarily primed polymerase chain reaction (AP-PCR) and ltx promoter PCR to molecularly characterise 35 A. actinomycetemcomitans Brazilian isolates: 21 of human origin and 14 from captive marmosets (Callitrix spp., primates commonly used as animal models for periodontal research). The discriminative capacity of each of 12 arbitrary primers was found to be variable, yielding between 3 and 24 PCR amplitypes. Combination of the results for all primers led to characterisation of 14 genotypes that grouped into four major clusters based on genetic similarity. Clusters 2, 3, and 4 were discriminative to host origin. A correlation with periodontal disease was suggested for strains belonging to clusters 3 and 4. The JP2-like PCR amplification pattern, associated with highly leukotoxic strains, was exclusive to human isolates and present in 29% of human isolates where it occurred in close relationship with AP genotypes L and J (cluster 3).

Cage Use and Feeding Height Preferences of Captive Common Marmosets (Callithrix j. jacchus) in Two-Tier Cages

Determining appropriate feeding regimes has important welfare implications for captive primates. This study examined the preference of food bowl heights in 6 pairs of common marmosets (Callithrix jacchus) housed in a 2-tier cage system. Given that marmosets are arboreal and spend most of their time in the upper half of their cages, we predicted that the marmosets would prefer a food bowl positioned at the top of the cage over one positioned at the bottom. We further predicted that this would be more apparent for the marmosets housed in lower tier than upper tier cages. Given a choice regarding where to feed, marmosets did prefer the top bowl to the bottom bowl; however, when only 1 food bowl was presented, its position had no significant effect on the marmosets' feeding behavior. In addition, contrary to the prediction, there were few differences in the marmosets' feeding behavior in the upper and lower tier cages. Feeding the marmosets in a bowl at the bottom of their cage did not result in greater cage use. On the basis of this study, we recommend positioning captive marmosets' food bowls high in the cage.

Ilheus arbovirus in wild birds (Sporophila caerulescens and Molothrus bonariensis)

To report the first Ilheus arboviruses isolated from wild birds and analyze its public health impact. Wild birds and mammals were captured using mist nets and Tomahawk traps, respectively. Blood samples were drawn from these animals and inoculated intracerebrally in Swiss suckling mice found in the Parque Ecológico do Tietê, Brazil. The isolates were identified by serological tests, such as hemagglutination, hemagglutination inhibition, complement fixation and neutralization. Besides virus isolation, serum samples were also tested for the presence of hemagglutination inhibition antibodies. Two strains of Ilheus virus were isolated from the bird species Sporophila caerulescens and Molothrus bonariensis. Specific antibodies to Ilheus virus were detected in serum samples of some birds (Columbina talpacoti, Geopelia cuneata, Sicalis flaveola and Molothrus bonariensis), marmosets (Callithrix jacchus and Callithrix penicillata) and coati (Nasua nasua). Virus isolation and detection of specific antibodies in serum samples of local, migratory and captive birds, captive marmosets and wild coati corroborate the circulation of Ilheus virus in the Parque Ecológico do Tietê. The migrating behavior of some species of wild birds, like Sporophila caerulescens, enables the virus spread to other regions. Taking into consideration its human pathogenicity and the presence of the virus in this area, local authorities should be aware of the risk of infecting the local community.

IgA-gliadin antibodies, IgA-containing circulating immune complexes, and IgA glomerular deposits in wasting marmoset syndrome.

Marmosets in captivity are highly susceptible to wasting marmoset syndrome (WMS), the aetiology of which is still not fully determined. The level of IgA-gliadin antibodies (IgA-AGA), of IgA-containing circulating immune complexes (IgA-CIC), and the degree of glomerular IgA deposits were compared between marmosets suffering from WMS and animals not affected by the disorder. Both IgA-AGA and IgA-CIC were demonstrable in all groups of monkeys investigated. IgA-AGA and IgA-CIC were significantly higher in monkeys with WMS than in non-affected animals. There was a significant correlation between the glomerular IgA-deposition and titre of IgA-AGA. The group of marmosets strongly positive for glomerular IgA deposits comprised significantly more animals suffering from WMS than the group without deposits. In the diet of the animals a considerable amount of gliadin-like cereal proteins was assayed. There are several parallels between the human disorders (coeliac disease and IgA-nephropathy/Berger's disease) and the changes observed in WMS. It should be further investigated if WMS in marmosets is a suitable animal model for both human diseases.

Allowing Captive Marmosets to Choose the Size and Position of Their Nest Box

AbstractPreferences for nest box size and position were tested in two groups of common marmoset, Callithrix jacchus jacchus. In a pre-test phase two, new, wooden nest boxes were introduced to each group alongside their old metal one, so that the animals could become familiar with them, and so that any pre-existing preference could be identified. In successive experiments: i) the old metal nest box was closed so that the marmosets had to choose a preferred box from the two new nest boxes; ii) the size of the preferred nest box was systematically reduced; and iii) in one of the groups the reduced nest box was restored to full size, but its position interchanged with the non-preferred box. In a further experiment, the position of the preferred, and then of the non-preferred box was raised to the highest point in the cage. The marmosets showed strong positional preferences which could not have been predicted without performing the tests. One of the groups also showed a strong preference for the high nest box. It was concluded that marmosets may exhibit preferences for their cage furniture, the basis of which may not be clear to us. These preferences should, however, be taken into account when designing cages to maximize the welfare of the animals.

Visual scanning by common marmosets (Callithrix jacchus): Functional aspects and the specialrrole of adult males

The rates of visual scanning and vocalizations were studied in a group of captive marmosets (Callinthrix jacchus) after the presentation of five different stimuli (artificial flower, playback of long calls, female/male conspecific, stuffed wild cat) in order to assess the function of visual scanning. Only the presentation of a stuffed cat induced a significant response. The adult males in particular increased their scanning rate and all adult individuals decreased their rate of vocalizations. The results indicate that visual scanning in marmosets is an appropriate measure of vigilance which seems to serve the function of predator detection and avoidance. The strong response of adult males suggests that they play a special role in predator detection.