Severe Intragroup Aggressions in Captive Common Marmosets (Callithrix jacchus)

Members of captive colonies of common marmosets (Callithrix jacchus), a small New World primate, can occasionally be victims of repeated, and potentially fatal, attacks by a family-mate. This study examined the records of a colony, looking for past instances of such aggressions. The aim was to better understand the possible causes underlying this phenomenon and to identify variables that could minimize their occurrence. The results showed that both males and females behaved as aggressors at the same rate, but females attacked just females, whereas males attacked both males and females. Most aggressions involved siblings and occurred at a higher rate when the cages were occupied by more than 5 nonhuman animals. The influence of group size was significant only when females behaved as aggressors. This study suggests that several factors can determine the occurrence of these aggressions and that their relative importance depends on the sex of the aggressor. The results of this study highlight the importance of collecting further data to verify whether crowding in a confined space, rather than group size per se, affects the incidence of these aggressions.     

Body Weight of Wild and Captive Common Marmosets (Callithrix jacchus)

Captive studies and occasional trappings of wild individuals indicate that callitrichids have small size and body weight and lack sexual dimorphism. We compared body weights of captive and wild Callithrix jacchus obtained by repeatedly weighing subjects from two populations in Brazil. We obtained captive data by routinely weighing 138 individuals from the Universidade Federal do Rio Grande do Norte colony and wild data via regular trapping of 243 individuals in 15 free-ranging groups from IBAMA's field site in Nísia Floresta. We assigned all subjects to one of four age classes—infant, juvenile, subadult, and adult—according to their birth dates or size, reproductive status, and dental development. There is no significant difference between males and females in any of the four age classes, but captive subjects were heavier than wild ones in all age classes but infant. Reproductive and nonreproductive adult females showed no statistical difference in weight. These results accord with previous reports of lack of body size sexual dimorphism in common marmosets and suggest that differences between wild and captive common marmosets are not constitutional, but are instead a consequence of diet and physical activity. The absence of weight difference between reproductive and nonreproductive females suggests that any possible advantage from high rank is outweighed by the costs of reproduction in common marmosets.     

Correction to: Evidence for Dialects in Three Captive Populations of Common Marmosets (Callithrix jacchus)

International Journal of Primatology - A Correction to this paper has been published: https://doi.org/10.1007/s10764-020-00196-x     

Locomotor Activity Rhythm in Free-ranging Common Marmosets (Callithrix jacchus)

Locomotor activity rhythm in the common marmoset has been well described and characterized in captivity, but there is no information about rhythmic aspects of this behavior in free-ranging conditions. To investigate if the locomotor activity rhythm in free-ranging common marmosets is similar to that found in captive common marmosets, we observed reproductive animals from two groups that inhabited at the Experimental Forestry Station, in northeastern Brazil (6°5'S, 35°12'W). From December 1992 to October 1993 we recorded the frequency of locomotor activity by focal animal sampling. The records of locomotor activity were submitted to spectral analysis and to the Cosinor test. Common marmosets showed an average duration of the active phase of 11:37 h ± 13.8 min. Similar to recorded in captive common marmosets, circadian rhythmicity was found with peaks in the morning, and in the afternoon, characterizing a bimodal pattern with peaks separated by 8 hours. The presence of a rhythmic pattern in the locomotor activity in free-ranging and captive common marmosets suggests that this pattern is not determined by the environmental conditions in captivity, but it has a endogenous component that play an important role for adaptation of this species to different conditions.     

Diurnal Variation in Scent Marking Behavior in Captive Male and Female Common Marmosets, Callithrix jacchus

Chemical communication by scent-marking behavior in New World primates is used to prevent the access of potential competitors to a territory, to identify food resources and the reproductive condition of mates, among others. In common marmosets, primates of the Callitrichidae family, this behavior also occurs as olfactory identification of an individual or of the reproductive status of females. Despite this information, the diurnal variation and gender differences in the profile of this behavior remain to be investigated. The aims of this study were to establish the diurnal profile of the distribution of this behavior and the influence of the sex of markers. We used 18 adult common marmosets, Callithrix jacchus, 10 males and 8 females from 6 family groups (6 fathers and 4 sons; 4 mothers and 4 daughters). The frequency of scent-marking behavior was recorded for each animal over a period of 8 days, twice a week, for 4 weeks, starting when the animals left the nest box (approximately at 05:00 a.m.) until the end of the photophase, at about 05:00 p.m. A MANOVA test was performed to compare the frequency of scent-marking behavior at 2 hour intervals using pooled data for males and females. The results showed that significantly higher levels of scent-marking behavior occurred during the 03:00-05:00 p.m. interval compared to all other intervals. Lower values were recorded during the 11:00-13:00 interval and an effect of the sex factor was also found, with the values being higher for females than for males, although a significant difference was recorded only for the 07:00-09:00 interval. Minimal values for males were recorded during the 07:00-09:00 interval, whereas minimum values for females were recorded during the 11:00-13:00 interval. However, the highest values for both sexes continued to occur during the 15:00-17:00 interval. These results suggest that scent marking behavior in common marmosets has a preferential incidence at the end of the day and this might be occurring in association with feeding behavior. At this time these animals usually forage more to prepare for the night's fast. Since these animals can discriminate chemical clues as long as 24 hours after they have been left, the higher incidence of this behavior at this time probably will assure that the animals will localize feeding resources used on the preceding day. Significant elevation of scent marking behavior in females in relation to males was found only at 07:00-09:00 interval and seems to be associated with signalizing of reproductive status, preferential access to foraging or both.     

Diurnal Variation in Scent Marking Behavior in Captive Male and Female Common Marmosets,Callithrix jacchus

Chemical communication by scent-marking behavior in New World primates is used to prevent the access of potential competitors to a territory, to identify food resources and the reproductive condition of mates, among others. In common marmosets, primates of the Callitrichidae family, this behavior also occurs as olfactory identification of an individual or of the reproductive status of females. Despite this information, the diurnal variation and gender differences in the profile of this behavior remain to be investigated. The aims of this study were to establish the diurnal profile of the distribution of this behavior and the influence of the sex of markers. We used 18 adult common marmosets, Callithrix jacchus, 10 males and 8 females from 6 family groups (6 fathers and 4 sons; 4 mothers and 4 daughters). The frequency of scent-marking behavior was recorded for each animal over a period of 8 days, twice a week, for 4 weeks, starting when the animals left the nest box (approximately at 05:00 a.m.) until the end of the photophase, at about 05:00 p.m. A MANOVA test was performed to compare the frequency of scent-marking behavior at 2 hour intervals using pooled data for males and females. The results showed that significantly higher levels of scent-marking behavior occurred during the 03:00–05:00 p.m. interval compared to all other intervals. Lower values were recorded during the 11:00–13:00 interval and an effect of the sex factor was also found, with the values being higher for females than for males, although a significant difference was recorded only for the 07:00–09:00 interval. Minimal values for males were recorded during the 07:00–09:00 interval, whereas minimum values for females were recorded during the 11:00–13:00 interval. However, the highest values for both sexes continued to occur during the 15:00–17:00 interval. These results suggest that scent marking behavior in common marmosets has a preferential incidence at the end of the day and this might be occurring in association with feeding behavior. At this time these animals usually forage more to prepare for the night's fast. Since these animals can discriminate chemical clues as long as 24 hours after they have been left, the higher incidence of this behavior at this time probably will assure that the animals will localize feeding resources used on the preceding day. Significant elevation of scent marking behavior in females in relation to males was found only at 07:00–09:00 interval and seems to be associated with signalizing of reproductive status, preferential access to foraging or both.     

Spatial Distribution and Exploitation of Trees Gouged by Common Marmosets (Callithrix jacchus)

Resource distribution shapes many aspects of primate behavioral ecology. Though the spatial patterning of fruits, leaves, and insects has been explored among primate foods, comparatively less is known about exudate distributions. Tree exudates are a renewable resource, provide long-term evidence of exploitation, and may be selectively exploited to manipulate spatial distribution. We assessed the spatial patterning of trees gouged by common marmosets (Callithrix jacchus) to determine if they exhibit a uniform, random, or clumped distribution. We also asked whether marmosets selectively gouge trees in home range centers, which may afford them exclusive access to exudates. We explored whether spatial or physical characteristics of trees predict how intensely gouged trees were exploited. The mean nearest neighbor distance of gouged trees was significantly closer than expected for a random distribution and Ripley’s K-function showed that gouged trees were clumped across all spatial scales in our study area. Clumping may enable marmosets to reduce day and home ranges and facilitate repeated gouging of trees. Gouged trees were not closer to marmosets’ home range centers than peripheries, nor were centrally located trees more intensely gouged. Increased gouging intensity was associated with larger tree circumferences, although this effect was primarily driven by interspecific differences in circumference. Although marmosets may benefit from exploiting clumped exudates, they do not concentrate gouging in areas where they are more likely to gain exclusive access. Species-specific tree characteristics such as exudate quality and/or bark properties may play a larger role in determining gouging patterns than intergroup feeding competition.     

Characteristics of the Light-Induced Phase Response of Circadian Activity Rhythms in Common Marmosets,Callithrix j. jacchus [Primates-Cebidae]

Phase-response experiments using 1-h light pulses (LPs) of 1,100 lux applied under constant dim light of 0.3 lux were conducted with common marmosets, Callithrix j. jacchus, in order to obtain a complete phase-response curve established according to the common experimental procedure in a diurnal primate. Maximal phase delays of the free-running circadian activity rhythm (- 90 min) were induced by LPs delivered at circadian time (CT) 12; e.g., during the beginning of the marmosets' rest time, maximal advances (+ 25 min) were elicited by pulses administered during the late subjective night at CT 21. In contrast to rodents, neither regular transient cycles nor regular period responses resulted from LP applications at different phases. To check whether the underlying period length affects the phase response in primates as well, the marmosets' circadian timing system was entrained to 25 h by a lightrdark (LD) cycle of 12.5:12.5 h. The 1-h LPs were delivered during the first circadian cycle produced under constant dim light after the entraining LD periods. Here, LPs applied at CT 21 led to phase advances exceeding those measured during the steady-state free run. At CT 12, minor or no phase delays could be elicited. These findings show that the phase-shifting effect of LPs on the circadian system of marmosets is similar to that observed in other diurnal mammals. Some of the results indicate that in this diurnal primate, LP-induced phase shifts may be mediated in part by a light-induced increase in locomotor activity (arousal).     

Characteristics of the Light-Induced Phase Response of Circadian Activity Rhythms in Common Marmosets, Callithrix j. jacchus [Primates-Cebidae]

Phase-response experiments using 1-h light pulses (LPs) of 1,100 lux applied under constant dim light of 0.3 lux were conducted with common marmosets, Callithrix j. jacchus, in order to obtain a complete phase-response curve established according to the common experimental procedure in a diurnal primate. Maximal phase delays of the free-running circadian activity rhythm (- 90 min) were induced by LPs delivered at circadian time (CT) 12; e.g., during the beginning of the marmosets' rest time, maximal advances (+ 25 min) were elicited by pulses administered during the late subjective night at CT 21. In contrast to rodents, neither regular transient cycles nor regular period responses resulted from LP applications at different phases. To check whether the underlying period length affects the phase response in primates as well, the marmosets' circadian timing system was entrained to 25 h by a lightrdark (LD) cycle of 12.5:12.5 h. The 1-h LPs were delivered during the first circadian cycle produced under constant dim light after the entraining LD periods. Here, LPs applied at CT 21 led to phase advances exceeding those measured during the steady-state free run. At CT 12, minor or no phase delays could be elicited. These findings show that the phase-shifting effect of LPs on the circadian system of marmosets is similar to that observed in other diurnal mammals. Some of the results indicate that in this diurnal primate, LP-induced phase shifts may be mediated in part by a light-induced increase in locomotor activity (arousal).     

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.     

Circadian and Ultradian Periodicities of Grooming Behavior in Family Groups of Common Marmosets (Callithrix jacchus) in Captivity

Three families' groups of common marmosets were observed to describe the characteristics of their grooming rhythmicity, as the duration of the episodes of self- and social grooming made and received by the animals, in captivity under natural environmental conditions. Data were collected by focal animal sampling, at 20 min hourly intervals during 16 non-consecutive days, from January to March in 1994 (sunrise: 05:24 h ± 2 min; sunset: 17:34 h ± 1 min). Time series were obtained for each individual and for each family through hourly duration of grooming. Family time serie was obtained through the mean of its individuals time series. Spectral analysis revealed statistically significant circadian rhythms for all families and individuals. Ultradian components were detected in 50% of the families and in 46.7% of the animals. Acrophases of self- and social grooming calculated by Single Cosinor took place between 9:21 h and 10:39 h, for the families. For individuals self- and social grooming made and received, acrophases occurred from 8:35 h to 12:43 h. The confidence limits of acrophases did not show differences between the families and the individuals within the families, irrespective of their sex, age and reproductive condition, suggesting that this behavior has a stronger temporal marking. Grooming has circadian and ultradian components of rhythmicity in captive families' groups of common marmosets, under natural environmental conditions. Since only some animals showed the ultradian component, it may be consequence of social or environmental masking, or yet phenotypic plasticity of temporal genotype. Further studies are needed to test these possibilities.     

Circadian Variation with a Diurnal Bimodal Profile on Scent-Marking Behavior in Captive Common Marmosets (Callitrhix jacchus)

Scent-marking behavior is associated with different behavioral contexts in callitrichids, including signalizing a territory, location of feeding resources, and social rank. In marmosets and tamarins it is also associated with intersexual communication. Though it appears very important for the daily routine of the individuals, very few researchers have investigated distribution through the 24-h cycle. In a preliminary report, we described a preferential incidence of this behavior 2 h before nocturnal rest in families of common marmosets. We expand the data using 8 family groups (28 subjects), 8 fathers, 6 mothers, 8 nonreproductive adults (4 sons and 4 daughters), and 6 juvenile (3 sons and 3 daughters) offspring that we kept in outdoor cages under natural environmental conditions. We recorded the frequency of anogenital scent marking for each group during the light phase, twice a wk, for 4 consecutive wks, from March 1998 to September 1999. Cosinor test detected 24- and 8-h variations in 89.3% and 85.7% of the subjects, respectively, regardless of sex or reproductive status. The 8-h component is a consequence of the 2 peaks for the behavior, at the beginning and end of the light phase. Daily distribution of scent marking is similar to that others described previously for motor activity in marmosets. The coincident rhythmical patterns for both behaviors seem to be associated with feeding behavior, as described for callitrichids in free-ranging conditions, involving an increase in foraging activities early in the morning and shortly before nocturnal rest.     

Training Common Marmosets (Callithrix jacchus) to Cooperate During Routine Laboratory Procedures: Ease of Training and Time Investment

Streamlining purchasing in nonhuman animal shelters can provide multiple financial benefits. Streamlining shelter inputs and thus reducing shelter costs can include trading paid labor and management for fewer, more involved volunteers or purchasing large quantities of medical supplies from fewer vendors to take advantage of bulk-purchasing discounts. Beyond direct savings, time and energy spent on purchasing and inventory control can be reduced through careful management. Although cost-cutting measures may seem attractive, shelter managers are cautioned to consider the potential unintended consequences of short-term cost reduction measures that could limit revenues or increase costs in the future. This analysis illustrates an example of the impact of cost reductions in specific expense categories and the impact on shelter net revenue, as well as the share of expenses across categories. An in-depth discussion of labor and purchasing cost-reducing strategies in the real world of animal shelter management is provided.     

Effect of Removal from the Family Group on Feeding Behavior by Captive Callithrix jacchus

Common marmosets are omnivorous primates with a highly diversified diet. There is no study describing if and how the diet is learned. Infants get their first bits of solid food from other monkeys in the group, which suggests that they may need an introduction to food items by older individuals before including them in their diet. We assessed the acceptance of novel and familiar food items by common marmosets, both isolated and in their family groups. We tested adult, subadults and juveniles from 5 captive families while isolated and in their family groups. The test consisted of presenting for 10 min novel and familiar food items to isolated individuals or to the whole family. We recorded the latency to start eating and the number of food items ingested. When isolated, adults ate more novel and familiar food items than juveniles did. They also started eating sooner than juveniles did. When tested alone, all juveniles, except one, never tasted novel food, and juveniles ingested fewer familiar food items than adults did. When tested in their family groups, juveniles ingested more familiar and novel food than when they were isolated. Our results suggest that: 1. juvenile common marmosets show more food neophobia than adults do, especially when alone; 2. the family group may facilitate the acceptance of novel food items by juveniles; 3. the family group, besides promoting the acceptance of novel food, may also increase its ingestion; and 4. dietary acquisition in Callithrix jacchus involves social facilitation.     

Characteristics of the circadian activity rhythm in common marmosets (Callithrix j. jacchus)

The circadian activity rhythm of the common marmoset, Callithrix j. jacchus was investigated by long-term recording of the locomotor activity of 15 individuals (5 males, 10 females) from 1.5 to 8 years old, both under constant illumination and under LD 12:12. The mean period of the spontaneous circadian rhythm was 23.2 ± 0.3 h. Neither sex-specific differences nor a systematic influence of light intensity on the spontaneous period were observed, but the period was dependent on the duration of the trial and on the age of the individual. Due to the short spontaneous period, in LD 12:12 there was a distinct advance of the activity phase with respect to the light time and a masking of the true onset of activity by the inhibitory direct effect of low light intensity during the dark time. After an 8 h delay shift of the LD 12:12, re-entrainment of the circadian activity rhythm required an average of 6.8 ± 0.7 days; the average re-entrainment time after an 8 h phase advance of the LD cycle was 8.6 ± 1.3 day. This directional effect is ascribed to characteristics of the phase-response curve. No ultradian components were observed, either in the LD-entrained or the free-running circadian activity rhythm.     

Natural and Anthropogenic Hybridization in Two Species of Eastern Brazilian Marmosets (Callithrix jacchus and C. penicillata)

Animal hybridization is well documented, but evolutionary outcomes and conservation priorities often differ for natural and anthropogenic hybrids. Among primates, an order with many endangered species, the two contexts can be hard to disentangle from one another, which carries important conservation implications. Callithrix marmosets give us a unique glimpse of genetic hybridization effects under distinct natural and human-induced contexts. Here, we use a 44 autosomal microsatellite marker panel to examine genome-wide admixture levels and introgression at a natural C. jacchus and C. penicillata species border along the São Francisco River in NE Brazil and in an area of Rio de Janeiro state where humans introduced these species exotically. Additionally, we describe for the first time autosomal genetic diversity in wild C. penicillata and expand previous C. jacchus genetic data. We characterize admixture within the natural zone as bimodal where hybrid ancestry is biased toward one parental species or the other. We also show evidence that São Francisco River islands are gateways for bidirectional gene flow across the species border. In the anthropogenic zone, marmosets essentially form a hybrid swarm with intermediate levels of admixture, likely from the absence of strong physical barriers to interspecific breeding. Our data show that while hybridization can occur naturally, the presence of physical, even if leaky, barriers to hybridization is important for maintaining species genetic integrity. Thus, we suggest further study of hybridization under different contexts to set well informed conservation guidelines for hybrid populations that often fit somewhere between “natural” and “man-made.”     

Behavioral and Hormonal Analysis of Social Relationships Between Oldest Females in a Wild Monogamous Group of Common Marmosets (Callithrix jacchus)

Social organization in common marmosets (Callithrix jacchus) appears to be based on a hierarchy of dominance, in which dominant females limit the reproductive functioning of subordinates. Reduced fertility was documented for captive but not for wild females. We investigated social dynamics and hormonal profiles of females living in a wild group. We collected behavioral and hormonal data during 7 mo from the reproductive and two nonreproductive adult females (probably daughters), and their interactions with the reproductive male. The subjects lived in a monogamous group at Nísia Floresta field station in northeastern Brazil. We collected behavioral data as all day follows, once a week and fecal material twice a week. We analyzed fecal samples for cortisol and progesterone using enzyme immuno assay (EIA) techniques. During the first three months we monitored the reproductive female (GRE) and the oldest nonreproductive female, (GIO). After the disappearence of GIO, we monitored the next oldest subordinate adult female, (GRA). GRE had just given birth at the beginning of the study, and she gave birth 6 mo later. During the last 2 weeks of GRE's gestation, GRA showed elevated progesterone levels, indicating ovarian cycling. Cortisol levels from GRE and GRA reached very high levels then. During GRA's cycling period, her interactions with the reproductive male (GT) were lower than when she was not cycling. We saw sexual interactions only between GT and GRE. The results provide evidence that ovarian function in mature subordinate females might be affected by the reproductive condition of the dominant female.     

Metabolic Characterization of the Common Marmoset (Callithrix jacchus)

High-resolution metabolomics has created opportunity to integrate nutrition and metabolism into genetic studies to improve understanding of the diverse radiation of primate species. At present, however, there is very little information to help guide experimental design for study of wild populations. In a previous non-targeted metabolomics study of common marmosets (Callithrix jacchus), Rhesus macaques, humans, and four non-primate mammalian species, we found that essential amino acids (AA) and other central metabolites had interspecies variation similar to intraspecies variation while non-essential AA, environmental chemicals and catabolic waste products had greater interspecies variation. The present study was designed to test whether 55 plasma metabolites, including both nutritionally essential and non-essential metabolites and catabolic products, differ in concentration in common marmosets and humans. Significant differences were present for more than half of the metabolites analyzed and included AA, vitamins and central lipid metabolites, as well as for catabolic products of AA, nucleotides, energy metabolism and heme. Three environmental chemicals were present at low nanomolar concentrations but did not differ between species. Sex and age differences in marmosets were present for AA and nucleotide metabolism and warrant additional study. Overall, the results suggest that quantitative, targeted metabolomics can provide a useful complement to non-targeted metabolomics for studies of diet and environment interactions in primate evolution.