Comparative analysis of masseter fiber architecture in tree-gouging (Callithrix jacchus) and nongouging (Saguinus oedipus) callitrichids

Common marmosets (Callithrix jacchus) and cotton-top tamarins (Saguinus oedipus) (Callitrichidae, Primates) share a broadly similar diet of fruits, insects, and tree exudates. Common marmosets, however, differ from tamarins by actively gouging trees with their anterior teeth to elicit tree exudate flow. During tree gouging, marmosets produce relatively large jaw gapes, but do not necessarily produce relatively large bite forces at the anterior teeth. We compared the fiber architecture of the masseter muscle in tree-gouging Callithrix jacchus (n = 10) to nongouging Saguinus oedipus (n = 8) to determine whether the marmoset masseter facilitates producing these large gapes during tree gouging. We predict that the marmoset masseter has relatively longer fibers and, hence, greater potential muscle excursion (i.e., a greater range of motion through increased muscle stretch). Conversely, because of the expected trade-off between excursion and force production in muscle architecture, we predict that the cotton-top tamarin masseter has more pinnate fibers and increased physiological cross-sectional area (PCSA) as compared to common marmosets. Likewise, the S. oedipus masseter is predicted to have a greater proportion of tendon relative to muscle fiber as compared to the common marmoset masseter. Common marmosets have absolutely and relatively longer masseter fibers than cotton-top tamarins. Given that fiber length is directly proportional to muscle excursion and by extension contraction velocity, this result suggests that marmosets have masseters designed for relatively greater stretching and, hence, larger gapes. Conversely, the cotton-top tamarin masseter has a greater angle of pinnation (but not significantly so), larger PCSA, and higher proportion of tendon. The significantly larger PCSA in the tamarin masseter suggests that their masseter has relatively greater force production capabilities as compared to marmosets. Collectively, these results suggest that the fiber architecture of the common marmoset masseter is part of a suite of features of the masticatory apparatus that facilitates the production of relatively large gapes during tree gouging.     

Monitoring ovarian function in marmosets and tamarins by the measurement of urinary estrogen metabolites

Practical aspects of urinary estrogen analysis were considered with regard to establishing simple and reliable methods for monitoring ovarian function in marmosets and tamarins. Changes in the hormone:creatinine ratio in small volumes of urine from the common marmoset were significantly correlated with changes in 24-h excretion. Comparison of the metabolism and excretion of estrogens during the ovarian cycle in the common marmoset and cottontop tamarin revealed interesting species differences. High concentrations of conjugated estrone were measured in marmoset plasma, but estradiol 17β was the predominant estrogen in urine. In contrast, estrone was the most abundant estrogen measured in tamarin urine. Both species excreted very little estriol. Sulfates and glucuronides were present in urine in similar proportions before ovulation in the marmoset, although after ovulation sulfates were the more abundant. Conversely, most of the estrogens in tamarin urine appeared to be conjugated as glucuronides. Direct assay for estrone sulfate was applied to the measurement of urinary estrogen excretion during the ovarian cycle in a marmoset. The results compared well with those for total estradiol 17β after hydrolysis and ether extraction. The use of direct assays for conjugated estrogens in small volumes of urine is suggested as a practical method for monitoring ovarian function in marmosets and tamarins.     

Phylogeny of lion tamarins (Leontopithecus spp) based on interphotoreceptor retinol binding protein intron sequences

The evolutionary relationships of the lion tamarins (Leontopithecus) were investigated using nuclear interphotoreceptor retinol binding protein (IRBP) intron sequences. Phylogenetic reconstructions strongly support the monophyly of the genus, and a sister relationship between the golden lion tamarin, Leontopithecus rosalia, and the black lion tamarin, L. chrysopygus, to the exclusion of the golden-headed lion tamarin, L. chrysomelas. The most parsimonious evolutionary reconstruction suggests that the ancestral lion tamarin and the common ancestor of L. rosalia and L. chrysopygus had predominantly black coats. This reconstruction is not consistent with a theory of orthogenetic evolution of coat color that was based on coat color evolution in marmosets and tamarins. An alternative reconstruction that is consistent with metachromism requires that ancestral lion tamarins had agouti hairs.     

Naturally occurring Tyzzer's disease in cotton-top tamarins (Saguinus oedipus)

We noted naturally occurring infection with Clostridium piliforme (Tyzzer's disease) in 2 captive-reared cotton-top tamarins (Saguinus oedipus). Spontaneous Tyzzer's disease has been reported in multiple species of laboratory, domestic, and wild animals but is extremely rare in humans and nonhuman primates. Distinct from idiopathic colitis, which is common in cotton-top tamarins, these 2 tamarins had severe, transmural, necrotizing typhlocolitis accompanied by myocarditis and hepatitis. Abundant bacteria compatible with C. piliforme, the etiologic agent of Tyzzer's disease, were present adjacent to lesions in the cecum-colon, liver, and heart. Therefore, colitis caused by C. piliforme, although rare, should be included as a differential diagnosis in cotton-top tamarins and as a cause of postnatal mortality in this species.     

Breeding of the cotton-top tamarin Saguinus oedipus oedipus: A comparison with the common marmoset

A colony experienced in the successful breeding of thecommon marmoset acquired 15 cotton-top tamarins for breeding purposes over a period of 2 yrs. Data are presented on the breeding of the cotton-top and compared with the breeding of the common marmoset. The tamarins did not breed as successfully as the common marmosets. There were several reasons for this: Cotton-tops took longer to produce young on initial pairing, had a longer birth interval, and showed a high incidence of suspected infanticide and parental neglect. These factors are thought to be largely responsible for the relatively low reproductive potential of the cotton-top in captivity.     

Temperature-metabolism relations in the cotton-top tamarin (Saguinus oedipus) model for ulcerative colitis

Examination of temperature-metabolism relations found no significant differences between thermoregulation of temperature housed laboratory cotton-top tamarins (Saguinus oedipus) and wild tamarins in Colombia, S.A. The results indicate that tamarins do not acclimate to a temperate environment and are metabolically stressed at T_a less than 32°C. This is consistent with an hypothesis of chronic metabolic stress as a factor in the etiology of cotton-top tamarin colitis, which is restricted to captive populations and not found in wild tamarins.     

Differences among captive callitrichids in the digestive responses to dietary gum

Although many members of the Callitrichidae, a monophyletic family of small, New World monkeys, have been observed to feed on plant exudates, available field data support the generalization that pygmy and common marmosets (Cebuella pygmaea and Callithrix jacchus) feed on gums to a greater extent than most other callitrichids. Because microbial fermentation is required for vertebrates to digest gums, gum-feeding primates may react differently to dietary gum from their relatives that eat little gum. To test this hypothesis, digestion trials were conducted on animals from the two marmoset species, two tamarin species (Saguinus fuscicollis and S. oedipus), and a species of lion tamarin (Leontopithecus rosalia). These species span the range of body sizes within the Callitrichidae. All animals were fed two variations of a homogeneous diet, which differed only in that gum arabic was added to one. Transit time of digesta (TFA) and digestive efficiency (as measured by the coefficients of apparent digestibility of dry matter and energy [ADDM and ADE, respectively]) were compared between diets for each individual. As predicted, the digestive responses of marmosets differed from the responses of the other study species. In marmosets, TFA tended to be longer when gum was added to the diet, while TFA did not change in the other three species. Digestive efficiency decreased in tamarins and lion tamarins with the addition of gum to the diet; marmoset digestive efficiency was unaffected by diet. The results of this research are consistent with the hypothesis that marmosets have digestive adaptations that aid in the digestion of gum that other callitrichids lack. © 1996 Wiley-Liss, Inc.     

Sleeping habits of tamarins, Saguinus mystax and Saguinus fuscicollis (Mammalia; Primates; Callitrichidae), in north-eastern Peru

The sleeping habits of moustached tamarins, Saguinus mystax , and saddle-back tamarins, Saguinus fuscicollis , were studied in northeastern Peru. Five types of sleeping sites were distinguished: 1) Jessenia bataua palms; 2) tree hollows; 3) dense tangles of vegetation; 4) crotches; 5) open horizontal branches. Both tamarin species used Jesseniu-palms most frequently. Tree hollows ranked second in the saddle-back tamarins, but were never used by moustached tamarins. Sleeping sites of moustached tamarins were located significantly higher than those of saddle-back tamarins. Jessenia -palms used by moustached tamarins were significantly higher than palms from a random transect sample, but this was not the case for Jessenia -palms used by saddle-back tamarins. For both species, concealment seems to be more important than height above ground. The maximum number of subsequent nights spent in the same sleeping site was two in moustached tamarins and six in saddle-back tamarins. The two tamarin species did not compete for sleeping sites. While the general pattern of sleeping site selection conforms to hypotheses predicting safety from predators as a major factor, differences between the two tamarin species reflect general niche differences between them. Most sleeping sites are located in exclusively used parts of the home range. Moustached tamarins generally use sleeping sites that are close to the last feeding site of the afternoon. The distance between simultaneously used sleeping sites of moustached and saddle-back tamarins are generally close together, which helps to minimize time spent out of interspecific association.     

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.     

Intracardiac thrombosis and aortic dissecting aneurysms in mustached tamarins (Saguinus mystax) with cardiomyopathy

Spontaneous intracardiac thrombosis is rarely reported in animals, particularly nonhuman primates. The finding of 2 cases of intracardiac thrombi in mustached tamarins (Saguinus mystax) that died as a consequence of congestive heart failure prompted us to do a retrospective study to determine the frequency of this condition. Clinical records, necropsy reports, and tissues from 60 mustached tamarins that died or were euthanized between 1996 and 2009 were reviewed. Of the 60 monkeys whose cases were reviewed, 10 (16.6%) had intracardiac thrombi, and 4 (6.6%) had dissecting aortic aneurysms. Of the 10 animals with intracardiac thrombosis, 3 had left ventricular involvement alone; 4 monkeys had thrombi only in the right ventricle, and the remaining 3 animals exhibited thrombi in both ventricles. Myocardial fibrosis and chronic renal disease were common findings in affected animals. The causes of the intracardiac thrombosis in the tamarins in the present study are not known, but the clinical signs and gross and microscopic lesions suggest that congestive heart failure secondary to cardiomyopathy is the primary contributor. In addition, the cause of the aortic dissecting aneurysms in the tamarins in this study is not known. Further studies are required to determine whether factors including aortic curvature, genetic background, or hypertension-alone or in combination-play a role. To our knowledge, the current retrospective study is the first report of intracardiac thrombosis and aortic aneurysms in mustached tamarins.     

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.     

Moving callitrichid monkeys from cages to outside areas

To assess the important aspects of a large area for environmental enrichment, the behavior of families of common marmosets Callithrix jacchus and cotton-top tamarins Saguinus oedipus when in laboratory cages and when in much larger outside areas was compared. All animals avoided areas with little cover. The two tamarin families preferred an indoor cage to a large open area with little cover and consequently only showed a limited range of behavior when outside. When dense cover was provided to the marmoset family, they used this area extensively, showing a wider range of behavior than when in cages and shifting to less active behavior patterns. By feeding marmosets in a central area, it was possible to allow unlimited access to the outside while effectively containing them.     

Focal ulcerative ileocolitis with terminal thrombocytopenic purpura in juvenile cotton top tamarins (Saguinus oedipus)

A newly recognized syndrome characterized by an acute focal ulcerative ileocolitis, anemia and thrombocytopenic purpura in five juvenile cotton-top tamarins is described. The presentation and morphology of this syndrome is distinct from any other reported gastrointestinal disease reported in tamarins. Traditional etiologies such as viruses, ingested toxins, Campylobacter, Salmonella and Yersinia and Clostridium difficile are not considered likely etiologic agents. Nontraditional etiologies such as anaerobes or pathologic strains of Escherichia coli are now being considered. This syndrome is of potential significance to ongoing research into the etiology of idiopathic tamarin colitis.     

Demographic parameters and events in wild moustached Tamarins (Saguinus mystax)

This paper examines demographic events in the context of population structure and genetic relationships in groups of wild moustached tamarins (Saguinus mystax). We used a combination of long-term behavioral observations and genetic data from a total of eight groups from a population in northeastern Peruvian Amazonia. The mean group size was 6.0 (range = 4-9), including 2.5 adult males and 1.8 adult females. Within-group relatedness was generally high (r = 0.3), and most nonbreeding individuals were either natal or closely related to the respective same-sex breeder. The mean annual persistence of adults in the groups was 70% and 68% for males and females, respectively, and the reproductive tenure of one breeding pair lasted for at least 6 years. Migrations predominantly occurred after stability-disrupting events such as the immigration of new individuals and/or the loss of breeding individuals, or when groups were rather large. Migrations of both breeding and nonbreeding males and females occurred. Our results show that the hypothesis of Ferrari and Lopes Ferrari [Folia Primatologica 52:132-147, 1989] that tamarins live in smaller and less stable groups with lower relatedness compared to marmosets does not generally hold true. In contrast, we found that tamarin groups can consist of predominantly related individuals, and are stable as well. It is also apparent that a single demographic event can produce a chain of subsequent complex demographic changes.     

Species and subspecies specificity in urine and scent marks of saddle-back tamarins (Saguinus fuscicollis)

Saguinus fuscicollisproduces scent marks which consist mainly of a mixture of urine and the secretions of circumgenital scent glands. The present study investigates the ability of saddle-back tamarins to discriminate between scent material from conspecifics and corresponding material from other species and to differentiate material from two subspecies of Saguinus fuscicollis.When choices between urine samples from conspecifics and from guinea pigs and choices between urine samples from conspecifics and from common marmosets were offered, the tamarins investigated samples from conspecifics more frequently. Similar responses were obtained when choices between scent marks from saddle-back tamarins and from common marmosets and between scent marks from saddle-back and red-chested moustached tamarins were offered. The tamarins also discriminated between scent marks and between extracts of scent marks from Saguinus f. fuscicollisand Saguinus f. illigeri.In these choice tests, subjects of both subspecies tended preferentially to investigate material from Saguinus f. fuscicollis.The results of these studies show that urine and scent marks contain chemical cues on which recognition of conspecifics can be based. Moreover, the scent marks of closely related subspecies also offer cues which could enable the tamarins to discriminate between them.     

Reproduction of the emperor tamarin (Saguinus imperator) in captivity,with comparisons to cotton-top and golden lion tamarins

Little information has been published on the reproductive biology and behavior of the emperor tamarin (Saguinus imperator). We analyzed twelve years of data on emperor tamarins at the Los Angeles Zoo and made comparisons with data on cotton-top tamarins (Saguinus o. oedipus) and golden lion tamarins (Leontopithecus rosalia) from the same collection. Secondary sex ratios did not differ significantly from 50:50. Births were not strictly seasonal for any species. The number of infants reared had a significant effect on interbirth interval for all species, with shorter intervals when only one or no infants were reared, but females did sometimes conceive early in lactation. In emperor tamarin families, all fathers and most older siblings carried new infants, usually beginning within a few days after a birth. Previous exposure to younger siblings did not appear to be critical to the development of competent parental behavior by zooborn emperor tamarin females.     

Predation on Orthoptera and other orders in insects by tamarin monkeys, Saguinus mystax mystax and Saguinus fuscicollis nigrifrons (Primates: Callitrichidae), in north-eastern Peru

Kaytydids and related insects are an important component in the diets of moustached ( Saguinus mystax mystax ) and saddle-back tamarins ( Saguinus fuscicollis nigrifrons ). Based on preliminary data of captured prey, trends suggest that partitioning occurs regarding orthopterans as a limited food resource. Of species caputre as prey, only three were shared by both tamarin species. Saddle-back tamarins appeared to specialize more on understorey species (0-4 m), concentrating on pseudophylline katydids. Moustached tamarins incorporated a greater percentage of phaneropterine katydids from the lower to middle canopy into their diet of insects. Although most prey species were exposed to view during the diurnal feeding period of the tamarins, only the saddle-back tamarin fed on katydids that spend the day concealed from view within dead curled leaves. Differentiation of the prey spectrum may represent a critical pattern of niche differentiation in these two sympatric tamarin species, which show a high overlap in their plant food resources.     

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.     

Locomotor behavior and feeding ecology of the panamanian tamarin (Saguinus oedipus geoffroyi,callitrichidae, primates)

The Callitrichidae are a family of New World primates that exhibit a complex of behavioral and morphological characters reputedly similar to those of tree squirrels of the genus Sciurus.In particular, the locomotor behavior of tamarins and marmosets has been described as “squirrel-like. ” In this paper I describe a field investigation of the locomotor behavior and ecology of the Panamanian tamarin (Saguinus oedipus geoffroyi)and the redtailed squirrel (Sciurus granatensis).From January through August 1978, a total of 1200 hr was spent observing freeranging populations of tamarins and tree squirrels in an area of secondary forest on the Pacific Coast of Panama. Observations were made using an instantaneous time sampling technique. Individual activity records were collected on focal animals and recorded at 2.5-min intervals throughout the day. The following information was collected: (a) nature and structure of the substrate exploited, (b) activities on these supports and/or types of resources procured, and (c) body posture involved in the use of these supports. Data presented indicate major differences in substrate preference and positional behavior in tamarins and tree squirrels. Unlike squirrels, tamarins avoid vertical and sharply inclined supports during travel. Movements through the canopy is accomplished by a series of long leaps which begin and end on thin terminal supports. However, the Panamanian tamarin spent numerous hours clinging to large vertical trunks while feeding on plant exudate. Gums comprise 23.O% of the noninsect portion of the tamarin diet. The relationships between small body size, claw-like nails, substrate preference, and positional behavior are discussed. Claw-like nails enable this primate to exploit a food resource that would otherwise be inaccessible. The interrelationship between environment, behaviour, and morphology provides a frameworks from which to understand callitrichid adaptations. These adaptations are not convergent with those of the sciurid rodents. An earlier draft of this paper was presented at the 48th Annual Meeting of the American Association of Physical Anthropologists, San Francisco, April 1979.     

Quantitative genetic analysis of cranial morphology in the cotton-top (Saguinus oedipus) and saddle-back (S. fuscicollis) tamarins

Patterns of morphological variation play an important role in evolutionary diversification and are critical to an informed interpretation of interspecific differences. When patterns of genetic variation have not diverged substantially, it is possible to reconstruct the differences in selection which gave rise to morphological differences among extant species. Morphological variation patterns are compared between two tamarin species, the cotton-top tamarin (Saguinus oedipus) and the saddle-back tamarin (S. fuscicollis illigeri). Genetic, phenotypic, and environmental variance/covariance and correlation matrices were obtained for a series of 39 cranial characters in each species (cotton-top tamarin, N = 328; saddle-back tamarin, N = 209) and for the species combined using crania from individuals of known genealogical relationship. After accounting for the effects of estimation error on measures of matrix similarity, patterns of phenotypic, genetic, and environmental variation and correlation were found to be very similar across species and among the types of variance within species. Taking the saddle-back tamarins as the standard, cotton-top tamarins have been selected for an enlarged anterior temporalis attachment area and increased facial prognathism. In primates, an enlarged anterior temporalis muscle is associated with incisive food preparation, especially at wide gape.