Environmental Enrichment for New World Primates: Introducing Food-Irrelevant Objects and Direct and Secondary Effects

This study examined methods of environmental enrichment for zoo animals for 4 New World primate species: pygmy and Geoffrey's marmosets (Cebuella pygmaea and Callithrix geoffroyi), red-bellied tamarins (Saguinus labiatus), and golden- headed lion tamarins (Leontopithecus chrysomelus). Subjects were housed in groups at the Philadelphia Zoo. Baseline behavioral time budget data were collected, and stimulus objects were then introduced in succession to each enclosure. Each object included multiple manipulable subcomponents. Time budget data were collected while objects were in the enclosures, and subjects' contacts with objects were videotaped. Overall time budgets were significantly altered in only the red-bellied tamarins, the least active of the species, solely due to a shift from social grooming to passive social contact; when categories were collapsed into broader categories, this effect disappeared. Object contact occurred within the 1st hr for all species and ranged over nearly 2 orders of magnitude, from approximately 10 sec per subject (red-bellied tamarins) to approximately 700 sec per subject (Geoffrey's marmosets). Habituation was not evident within any 1st hr of observation but was shown when 1st hr observations were compared with those from subsequent days. This article discusses implications for environmental enrichment in zoos.     

Visual monitoring of threatening objects by captive tamarins (Saguinus labiatus)

Captive social groups of red-bellied tamarins (Saguinus labiatus) were observed in the presence of threatening, inanimate objects. The tamarins monitored the stimuli over the course of the 20-minute trials by conducting brief, periodic visual checks of the objects. The average number of checks per subject per trial was stable both across trials and between groups, and individual differences in rates varied relatively little around the group means. These data generate the hypothesis that there is a species-typical execution of vigilance in the presence of mildly threatening objects. This execution takes the form of brief visual inspections of the stimulus, usually by one tamarin at a time, at a fairly consistent rate. The discussion of the data takes place in the context of the behavioral ecology of callitrichid species.     

Gum feeder as environmental enrichment for zoo marmosets and tamarins

Tamarins and marmosets are small-bodied social callitrichines. Wild callitrichines feed on exudates, such as sap and gum; particularly, marmosets are mainly gummivores, while tamarins consume gums only occasionally and opportunistically. Zoo marmosets and tamarins are usually provided with gum arabic as an alternative to the exudates normally found in the wild. The aim of this study was to evaluate the effects of a gum feeder on the behavior and well-being of four zoo-managed callitrichines. We studied four cotton-top tamarins (Saguinus oedipus), four red-handed tamarins (S. midas), two pygmy marmosets (Cebuella pygmaea), and three Geoffroy's marmosets (Callithrix geoffroyi) housed at Parco Natura Viva (Italy). We conducted the study over two different periods, a baseline (control, without the gum feeder) and then a gum feeder (when the gum feeder was provided) period. We used continuous focal animal sampling to collect behavioral data, including durations of social and individual behaviors. We collected 240 min of observations per period per study subject, with a total of 3,120 min for all the subjects in the same period and of 6,240 min in both periods. We analyzed data by using nonparametric statistical tests. First, we found that the gum feeder promoted species-specific behaviors, such as exploration, and diminished self-directed behaviors, suggesting an enriching effect on tamarin and marmoset behavior. Moreover, in red-handed tamarins, the provision of the gum feeder reduced the performance of self-directed and abnormal behavior, specifically coprophagy. These results confirm that gum feeders are effective foraging enrichment tools for zoo marmosets and tamarins.     

Factors influencing weight changes in callitrichids at the Bronx zoo

Callitrichids are small monkeys with high metabolic rates who appear to be susceptible to spontaneous diseases and possibly to environmental changes creating challenges in maintaining them in captivity. This study investigates whether life events (i.e. medical, social and housing changes) can influence weight. In previous research, body mass has been shown to be correlated with periods of illness, group composition changes and stress. Weights of 56 individual callitrichid monkeys (20 marmosets, 26 tamarins and 11 lion tamarins) at the WCS's Bronx Zoo were examined over approximately 2½ years. Weight fluctuations were scored based on 5%, 10% and 1 standard deviation criteria during periods of medical (illness and injury), social (introductions and separations), housing (movement within or between buildings) events and during periods when no‐events occurred. Additionally, weights were examined for 3 months before and after periods of illness to look for trends in weight changes for 47 medical events (14 marmosets, 21 tamarins and 12 lion tamarins). Moreover, in five alloparenting males (four tamarins and one lion tamarin), weights were examined to determine if weight loss occurred after births as observed in earlier studies. The results show that a 5% and 1SD criterion may be too sensitive a criterion. We therefore deemed that a 10% weight loss may be the best criterion. For marmosets, a 10% weight loss occurred in association with all events. For tamarins, weight loss occurred with housing events. In lion tamarins, weight loss was observed with medical events. No significant weight loss was observed in alloparenting males. Zoo Biol 29:551–566, 2010. © 2009 Wiley‐Liss, Inc.     

Sex Differences in Olfactory Communication in Saguinus labiatus

We assessed behaviors involved with depositing and receiving scent in three captive heterosexual pairs of red-bellied tamarins (Saguinus labiatus). The frequencies of scent deposition and scent investigatory behaviors differed between the sexes. Females scent marked exclusively by the anogenital gland. Males deposited 95.8% of scent marks via the anogenital gland and 4.2% via the sternal gland. Females scent marked at a significantly higher rate than that of males (0.9 ± 0.1 versus 0.3 ± 0.1 per 20 min, respectively). Males investigated the scent of their opposite-sex partners whereas females investigated no male scent. Mean ± SEM latency for males to investigate female scent was 208.7 ± 65.0 sec. Around 9% of all scent marks were overmarked within 8 min and there was a nonsignificant trend for males to overmark the scent of their female partners than vice versa. We discuss the sex differences in olfactory communication in red-bellied tamarins in terms of sexual selection theory.     

Opportunistic Pneumocystis carinii infection in red-bellied tamarins (Saguinus labiatus).

P. carinii infection in red-bellied tamarins (Saguinus labiatus), born and maintained in a laboratory breeding colony, was examined by histopathologic examination postmortem. P. carinii cysts were detected in 6 of 10 red-bellied tamarins examined, by using Grocott's, toluidine blue O and immunostaining with avidin-biotin complex using antisera for rat-, simian-, and human-P. carinii. The results obtained from the present studies imply that P. carinii may be an important pathogen in this species.     

Treatment with CRH-1 antagonist antalarmin reduces behavioral and endocrine responses to social stressors in marmosets (Callithrix kuhlii)

Corticotropin-releasing hormone (CRH) has multiple roles in coordinating the behavioral and endocrine responses to a host of environmental challenges, including social stressors. In the present study we evaluated the role of CRH in mediating responses to a moderate social stressor in Wied's black tufted-eared marmosets (Callithrix kuhlii). Male and female marmosets (n=14) were administered antalarmin (a selective CRH-1 receptor antagonist; 50 microg/kg, p.o.) or vehicle in a blind, counterbalanced, crossover design. One hr after treatment, marmosets were separated from long-term pairmates and then housed alone in a novel enclosure for 7 hr. Behavior was recorded during separation and upon reunion with the partner, and urine samples for cortisol assay collected before, during, and after the intervention. Separation from partners elevated urinary cortisol concentrations over baseline for both conditions, but antalarmin treatment reduced the magnitude of the elevation. Antalarmin also lowered rates of behavioral patterns associated with arousal (alarm and "e-e" vocalizations, object manipulate/chew), but had no effect on contact calls, locomotory activity or alertness. Although most patterns of social behavior upon reunion with the partner were not affected by antalarmin, antalarmin-treated marmosets displayed more sexual behavior (mounts and copulations) upon reunion. These data indicate that antagonism of the CRH-1 receptor acts to reduce the magnitude of both endocrine and behavioral responses to a moderate social stressor without causing any overall reduction in alertness or general activity. This supports the hypothesis that CRH, acting through its type 1 receptor, is involved in coordinating the responses to anxiety-producing events. These results further suggest that the marmoset is a useful model for exploration of the role of CRH in mediating the behavioral and neuroendocrine responses to psychosocial stressors, particularly in the context of heterosexual social relationships.     

The regulation of maternal behaviour in marmosets and tamarins

This article reviews a long-term investigation into the roles of (1) experience obtained with infants during development and postnatally, and (2) levels of reproductive-steroid hormones during late pregnancy, in the regulation of maternal caregiving motivation and behaviour in the red-bellied tamarin (Saguinus labiatus) and the common marmoset (Callithrix jacchus) (family Callitrichidae, Order Primates). Both observational studies, e.g. post hoc analysis of the relationship between developmental caregiving experience and infant-rearing success, and manipulative studies, e.g. direct analysis of the effects of sex-steroid administration on maternal motivation, were performed. In red-bellied tamarins, a breeding female's infant-rearing success was related to its caregiving experience obtained during development and postpartum/postnatally. In multiparous females lacking developmental caregiving experience, postpartum maternal caregiving behaviour and infant-rearing success were related to prepartum urinary oestradiol levels. In nulliparous common marmosets, caregiving of infant-siblings increased as a consequence of physical interaction with parent-infant dyads, late pregnancy, and exposure to late pregnancy-like levels of progesterone and oestradiol. The evidence for a dual mechanism of endocrine and experiential regulation of caregiving in these monkeys is discussed in terms its evolution and function.     

The ecology and evolution of patience in two New World monkeys

Decision making often involves choosing between small, short-term rewards and large, long-term rewards. All animals, humans included, discount future rewards--the present value of delayed rewards is viewed as less than the value of immediate rewards. Despite its ubiquity, there exists considerable but unexplained variation between species in their capacity to wait for rewards--that is, to exert patience or self-control. Using two closely related primates--common marmosets (Callithrix jacchus) and cotton-top tamarins (Saguinus oedipus)--we uncover a variable that may explain differences in how species discount future rewards. Both species faced a self-control paradigm in which individuals chose between taking an immediate small reward and waiting a variable amount of time for a large reward. Under these conditions, marmosets waited significantly longer for food than tamarins. This difference cannot be explained by life history, social behaviour or brain size. It can, however, be explained by feeding ecology: marmosets rely on gum, a food product acquired by waiting for exudate to flow from trees, whereas tamarins feed on insects, a food product requiring impulsive action. Foraging ecology, therefore, may provide a selective pressure for the evolution of self-control.     

Blood chemistry of the common marmoset (Callithrix jacchus) maintained in an indoor-outdoor environment: Primate comparisons

Blood chemistry values were collected over a three-year period from at least 10 colony-born and 24 wild-born apparently normal common marmosets. BUN, SGOT, creatinine, calcium, phosphorus, alkaline phosphatase, protein, albumin, cholesterol, triglycerides, uric and glucose values were determined. A statistical comparison of baseline values was made between wild-born, colony-born, male and female marmosets. Also the same comparison was made between common marmosets and cotton-top tamarins, white lipped tamarins and human subjects.     

Red-bellied tamarins (Saguinus labiatus): Hematologic reference values and hemopathologic responses

Hematologic reference values have been established for captive adult red-bellied tamarins (Saguinus labiatus) by carrying out full blood counts and fibrinogen estimations on 25 clinically normal animals. The only significant sex difference detected was in the reticulocyte count which was higher in females than in males. The reference values were used to identify abnormal changes in the blood of nine clinical cases. Hypochromic anemia, neutrophilia, and raised fibrinogen levels were found in animals with self-inflicted injuries, dermatitis, and ileocecal intussusception. Target cells and jaundiced plasma were noted in a case of yersiniosis. Two animals in which generalized muscle wasting was the main abnormal clinical sign were severely anemic, and in one of these cases a significant number of Heinz bodies was present. The findings in these two animals were compared with those in common marmosets (Callithrix jacchus) with possible wasting marmoset syndrome.     

Spontaneous pathology of the common marmoset (Callithrix jacchus) and tamarins (Saguinus oedipus, Saguinus mystax)

Background  Marmosets and tamarins are increasingly used in research, but their pathology remains poorly defined compared with Old World primates.

Methods  Necropsy records of 129 marmosets and 52 tamarins were reviewed; none was used experimentally.

Results  The most common marmoset lesions were dehydration, emaciation, nephritis, colitis, and inanition. The most common tamarin lesions were dehydration, ascites, emaciation, and congestive heart failure. Colitis and heart disease were the most common cause of death in marmosets and tamarins, respectively. Immature marmoset and tamarin deaths often occurred within the first month of life. Immature marmosets usually died from inanition, stillbirth, and colitis; immature tamarins from atelectasis, stillbirth, heart failure, and colitis. Lymphoma was the most common neoplasm for both marmosets and tamarins.

Conclusion  The findings were similar to prior reports with differences in frequency and severity. We report the first case of endometriosis in a marmoset.     

Taste thresholds and above-threshold responses to fructose solution in relation to diet in Callitrichidae primates]

Taste thresholds and consumption responses to above-threshold concentrations of fructose solutions were determined in eight callitrichid primate species using the "two-bottle preference test". Although taste thresholds are relatively similar across species, above-threshold responses may differ considerably between marmosets and tamarins. As fructose concentration increases, the rate of consumption increases less for most marmoset species (Cebuella and Callithrix spp.) than for Goeldi's monkey (Callimico) and tamarins (Saguinus and Leontopithecus spp.). It is proposed that distinct shapes of the curves illustrating these responses characterize species in terms of global taste system adaptations to different diets.     

Will travel for food: spatial discounting in two new world monkeys

Nonhuman animals steeply discount the future, showing a preference for small, immediate over large, delayed rewards. Currently unclear is whether discounting functions depend on context. Here, we examine the effects of spatial context on discounting in cotton-top tamarins (Saguinus oedipus) and common marmosets (Callithrix jacchus), species known to differ in temporal discounting. We presented subjects with a choice between small, nearby rewards and large, distant rewards. Tamarins traveled farther for the large reward than marmosets, attending to the ratio of reward differences rather than their absolute values. This species difference contrasts with performance on a temporal task in which marmosets waited longer than tamarins for the large reward. These comparative data indicate that context influences choice behavior, with the strongest effect seen in marmosets who discounted more steeply over space than over time. These findings parallel details of each species' feeding ecology. Tamarins range over large distances and feed primarily on insects, which requires using quick, impulsive action. Marmosets range over shorter distances than tamarins and feed primarily on tree exudates, a clumped resource that requires patience to wait for sap to exude. These results show that discounting functions are context specific, shaped by a history of ecological pressures.     

Haematological, coagulation and blood chemistry data in red-bellied tamarins Saguinus labiatus

Haematology, coagulation and clinical chemistry data are reported for a group of male and female red-bellied tamarins (Saguinus labiatus). The tamarins were juvenile and young adults and were bred in captivity. High mean values for activities of alkaline phosphatase, alanine amino-transferase, aspartate aminotransferase and creatine kinase were noted. The findings are compared with data obtained from other members of the family Callitrichidae.     

Does the milk of callitrichid monkeys differ from that of larger anthropoids?

The generalization that anthropoid primates produce dilute milks that are low in protein and energy is based primarily on data from large monkeys of the families Cebidae and Cercopithecidae, as well as humans. The marmosets and tamarins (Callitrichidae) are not only much smaller in body size, but also typically raise multiple offspring during a relatively brief lactation. We hypothesized that selection for small body size and high reproductive rate might favor secretion of milk of higher energy and protein concentrations. To test this hypothesis, 46 milk samples collected from 10 common marmosets (Callithrix jacchus, ca. 350 g) were assayed for dry matter (DM), crude protein (CP), fat, and sugar; and gross energy (GE) was calculated from these constituents. We also assayed five samples collected from three golden lion tamarins (Leontopithecus rosalia, ca. 700 g) and six samples collected from a single pygmy marmoset (Cebuella pygmaea, ca. 150 g) over two lactation periods. All samples were collected between days 10 and 57 post partum, representing mid lactation for these species. The milks of these three species were similar, containing 14.0%, 16.1%, and 13.7% DM; 2.7%, 2.6%, and 2.9% CP; 3.6%, 5.2%, and 3.7% fat; 7.4%, 7.2%, and 7.8% sugar; and 0.76, 0.90, and 0.82 kcal/g for common marmosets, golden lion tamarins, and the pygmy marmoset, respectively. These species produced milks with energy values that were within the range reported for large anthropoids, albeit with slightly higher protein concentration. However, milk composition did vary substantially among individual common marmoset females, especially in the proportion of milk energy derived from fat. In contrast, CP as expressed as a percent of GE was remarkably constant among common marmoset females. Callitrichid milk appeared to be similar to that of larger anthropoid primates in GE, but was higher in CP and in the proportion of GE from CP. However, the small sample sizes for the golden lion tamarin and the pygmy marmoset, and the wide variation in milk composition found among common marmoset females cautions against definitively characterizing the milks of callitrichids from these data.     

Behavioral and hormonal response of common marmosets, <Emphasis Type="Italic">Callithrix jacchus</Emphasis>, to two environmental conditions

Captive animals of several species change their behavioral pattern and hormonal profile in response to physical (for example, cage size and temperature) and social (for example, group size and social isolation) modification of their environment. To evaluate the effect of environmental change in captivity, the affiliative (contact/proximity and allogrooming) and individual (approach, leaving, scent mark, locomotion, and autogrooming) behavior of five family groups of common marmosets, Callithrix jacchus, were recorded on weekdays (non-quiet) and at the weekend (quiet) for two months. In addition, fecal samples were collected for four of these groups to measure their cortisol levels under both conditions. The behavioral pattern and hormonal profile of breeding pairs and their offspring were modified by different management routines used in the experimental conditions. We found that the animals spent more time in affiliative interactions at the weekend, whereas on weekdays, they showed more individual behaviors. Moreover, cortisol levels of breeding pairs and their offspring were higher on weekdays, suggesting that common marmosets living in captivity react to environmental modification by changing their behavioral and hormonal pattern.     

Vigilance in Single- and Mixed-Species Groups of Tamarins (Saguinus labiatus and Saguinus fuscicollis)

By forming larger sizes of groups, individuals benefit from a decrease in vigilance, but the collective vigilance of the group as a whole is not compromised. We examined whether this group size effect is apparent in mixed-species groups of red-bellied tamarins (S. labiatus) and saddleback tamarins (S. fuscicollis) which form stable and permanent associations in the wild. We studied general vigilance and responses to hidden threatening stimuli in five captive groups of each species, while they were housed in single- and mixed-species groups. For vigilance, the individual rate was lower in the larger mixed-species groups than in the smaller single-species groups. In addition, the amount of time when at least one individual was vigilant was higher in mixed-species groups. This suggests that the tamarins alter their vigilance behavior in the presence of the other species. In response to hidden threats, both species performed brief vigilance checks and frequencies of checking did not differ in single- and mixed-species groups. However, both species had a significant reduction in the mean duration per check, and there was a reduced total amount of time spent vigilance checking in the mixed-species groups compared to the single-species groups, demonstrating the group size effect. Overall the mixed-species groups had a higher number and mean duration of checking than the smaller single-species groups. Given that the two species share a common set of predators, and respond to each other's alarm calls, these findings provide strong evidence that individuals of both tamarin species may be able to benefit from forming mixed-species groups via improved vigilance and monitoring of threats.     

Sleep quantitation in common marmoset, cotton top tamarin and squirrel monkey by non-invasive actigraphy

Sleep quantitation data on the Neotropical primate species, apart from the squirrel monkey, are still sparse. As such, we have quantitated sleep in the common marmosets (Callithrix jacchus), cotton top tamarins (Saguinus oedipus) and squirrel monkeys (Saimiri sciureus) reared in one primate facility simultaneously, by non-invasive actigraphy. The range in total sleep time/24h measured for male adult common marmosets, cotton top tamarins and squirrel monkeys were 713-793 min (n=4), 707-889 min (n=4) and 459-475 min (n=2) respectively. The range in sleep episode length /12h dark phase for marmosets, tamarins and squirrel monkeys were 21-52 min (n=3), 10-28 min (n=4) and 9-15 min (n=2) respectively. Since vigilance is a critical evolutionary adaptive feature of predator avoidance among Callitrichid monkeys and squirrel monkeys, the shorter ranges in sleep episode length recorded, even under captivity, in this study could be interpreted as probable indicators of such vigilance behavior during the rest phase. We hypothesize that the vigilance behavior when it exists during a primate's active phase should also prevail when it is at rest (sleep). This hypothesis deserves additional testing in female Callitrichid monkeys.