Evidence of hybrid vigor in subspecific hybrids of the saddle-back tamarin (Saguinus fuscicollis)

The effect of hybridization on infant survival was investigated in subspecific crosses of the saddle-back tamarin (Saguinus fuscicollis) at the Oak Ridge Associated Universities (ORAU) Marmoset Research Center (Oak Ridge, TN). Cox Proportional Hazards Regression was used to compare infant survival between (1) pure subspecies, (2) F1, F2, and backcrossed hybrids, and (3) hybrids and their parental subspecies. Also, effects of management changes, sex, and litter size on infant survival were investigated. There were no significant differences in infant survival between the pure subspecies. Also, degree of hybridization (F1, F2, or backcross) did not have a significant effect on infant survival. Progeny of hybrid crosses between S. f. lagonotus and S. f. illigeri was found to have significantly (P < 0.05) higher infant survival than both of their parental subspecies. Individuals born after diet and management changes in the colony had significantly (P < 0.05) higher survival than those born before. There were no significant sex differences in infant survival. Individuals born into triplet litters had significantly (P < 0.05) lower survival than those born into twin litters. These results show heterosis (hybrid vigor) for infant survival in one subspecific S. fuscicollis cross (S. f. lagonotus × S. f. illigeri). The results suggest genetic divergence between the subspecies populations and possible reproductive isolation in the wild. © 1994 Wiley-Liss, Inc.     

Endocrine monitoring of the ovarian cycle and pregnancy in the saddle-back tamarin (Saguinus fuscicollis) by measurement of steroid conjugates in urine

Direct measurements of urinary immunoreactive estrone conjugates (E1C) and pregnanediol glucuronide (PdG), were applied to monitoring the ovarian cycle (n = 9) and pregnancy (3 full term pregnancies, 2 mid-term abortions) in Saguinus fuscicollis. During the ovarian cycle, urinary E1C concentrations revealed a high degree of day-to-day variability and appeared to be uninformative in reflecting cyclic ovarian function. In contrast, PdG was a reliable indicator of ovarian cyclicity with excretion patterns corresponding well with plasma progesterone profiles. Luteal phase PdG concentrations were on average 4–7–fold higher than corresponding follicular phase values. On the basis of changes in circulating progesterone, a mean cycle length of 25.7 ±1.0 days with an average follicular phase of 7.1 ± 0.6 days and a mean luteal phase of 18.6 ± 0.7 days, was found (n = 14 cycles). Following conception, both urinary steroid conjugate concentrations increased and elevated levels were maintained beyond the normal luteal phase length, allowing pregnancy to be determined at around day 25–30. During mid- to late pregnancy, PdG levels declined while E1C concentrations continued to be elevated until approximately 6 weeks before parturition when a decrease occurred. Both hormones showed a clear and rapid fall to follicular phase values following termination of pregnancy at either parturition or mid-term abortion. Post partum ovulations (n = 5) occurred on average 17–18 days following birth with four ovulations leading to conceptions. The results demonstrate the potential of urinary steroid conjugate analysis as a practical and reliable method for non-invasive monitoring of reproductive status in the female saddle-back tamarin. © 1995 Wiley-Liss, Inc.     

Social influences on first reproductive success and related behaviors in the saddle-back tamarin (Saguinus fuscicollis,callitrichidae)

Some aspects of sociosexual behavior and the age at which maturing females experienced their first evident pregnancy and at which maturing males caused their first evident pregnancy were recorded in Saguinus fuscicolliscohabiting from 6 months of age with either an adult or a maturing sex partner. The following pair combinations and trios were studied: young male -young female, young male-adult female, adult male-young female, and adult male-young male-young female. The most frequent type of social interaction between young animals was rough and tumble play, while huddling was the most frequent interaction between young animals and their adult partners. Grooming and sexual interactions were very infrequent and there were no differences in the frequencies of these interactions among subject groups. Maturing females cohabiting with an adult male conceived significantly earlier than maturing females cohabiting with a male of their own age. Maturing males cohabiting with adult females sired offspring at a significantly earlier age than males cohabiting with a female of their own age. Some possible behavioral and physiological processes involved in the causation of early reproductive success in young tamarins cohabiting with adults are discussed. Saguinus fuscicollis fuscicollis andSaguinus fuscicollis illigeri.     

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.     

Sexual and social behavior of adult saddle-back tamarins (Saguinus fuscicollis), castrated as neonates

The behavior of four adult males castrated as neonates was compared with that of three neonatally sham-castrated males and two untreated males serving as controls. Two males castrated as sexually experienced adults served as additional controls. All males lived in permanent male-female pairs. The interactions of neonatally castrated, sham-castrated, and intact control males with strange conspecifics were tested in a situation analogous to territorial defense. In addition, the interactions of all males with their female pair mates were tested. Neonatally castrated males showed less injurious aggression against strangers and interacted with them less frequently than control males. There were significant differences between both groups of males in some of the agonistic behaviors recorded, but not in all. In pair tests, neonatally castrated males failed to show any coordinated male copulatory behavior but control males did. Males castrated as adults showed rates of mounting and thrusting similar to those of intact controls. Neonatally castrated males tended to interact with their females on a lower level than neonatally sham-castrated and untreated control males. How ever, most differences between both groups in the levels of pair mate interactions were not statistically significant. It is concluded that castration during neonatal life prevents the display of male copulatory behavior in adulthood and selectively affects the display of a number of other behaviors in adulthood. It is not possible at this point to decide whether these results are due to hormonal deficiencies on an organizational or activational level or both. However, data from studies currently in progress suggest that organizational processes might be responsible for part of the effect.     

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.     

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.     

Age-related changes in ovarian morphology of the South American tamarin Saguinus fuscicollis (Callitrichidae)

The aim of this histological study was to investigate the postnatal ontogeny of the ovaries in Saguinus fuscicollis to provide a detailed knowledge of the ovarian morphology for further endocrinological studies. Gonads from 43 animals between one day and 18 years of age were investigated. Based on the available material the ovarian development is characterized by seven distinct stages. 1. Neonatal stage : Folliculogenesis is still in progress. The ovarian medulla is filled with an intraovarian rete system, which forms open connections between the rete tubules and the cords containing oocytes. 2. Infantile stage : One month after birth the ovarian cortex is mainly composed of primordial follicles and a few primary follicles at the corticomedullary border, which are separated from each other by connective tissue. At two months, folliculogenesis is nearly completed. The first secondary follicles are present. 3. Juvenile stage : In six-month-old females weighing 184±9.5 g, folliculogenesis has reached the stage of secondary follicles with up to six layers of granulosa cells. In females of the same age weighing 251.5±37 g, antral follicles attain a maximum diameter of 925 μm m. 4. Pubertal stage : At the age of 8–10 months, corpora lutea accessoria (CLA) begin to form from atretic antral follicles. 5. Adult stage : The ovaries of all females older than 1.2 years are filled with large patches of interstitial gland tissue (IGT). In breeding females up to 58.4%of the antral follicles are intact. In non-breeding daughters living in the family group only 1.8%are intact, the rest are in various stages of atresia and form CLA. 6. Climacterial stage : With increasing age (8–13 years), the number of intact follicles decreases dramatically and IGT fills nearly the whole ovary. 7. Senile stage : In females older than 14 years, nearly all remaining follicles show signs of atresia.     

Saddle-back tamarin (Saguinus fuscicollis) reproductive strategies: Evidence from a thirteen-year study of a marked population

We monitored a population of four to seven groups of individually marked saddle-back tamarins (Saguinus fuscicollis; Callitrichidae) at the Cocha Cashu Biological Station in Peru's Manu National Park every year from 1979 through 1992. In this paper we use data on life histories, group compositions, group formations, and dispersal patterns collected during these 13 years to examine the reproductive strategies of males and females. Group compositions and mating patterns were quite variable in this population, with both monogamy and cooperative polyandry common. In polyandrous groups, two males shared a female's copulations and cooperatively cared for her young. Although most groups contained a single breeding female, we recorded four cases in which secondary females successfully reared young. Most young females appeared to wait in their natal groups for the first opportunity to fill a primary breeding position in their own or a neighboring group. Females that acquired primary breeding positions maintained those positions for a mean of 3 years. No female was observed to transfer between groups a second time. Variation in female lifetime reproductive success was high. Half of the females marked as juveniles never bred; the other half produced an average of 3.5 young. A paucity of female breeding opportunities may explain the high mortality of females between 2.5 and 4.5 years of age and the resulting male-biased adult sex ratio. The majority of groups contained more than one probable male breeder. Polyandrous groups included both related and unrelated males. Behavioral differences between Cocha Cashu tamarins and other studied populations may result from the pressures of living in an environment inhabited by nine other primate species and numerous predators. © 1996 Wiley-Liss, Inc.     

Foraging behavior of a tamarin group (Saguinus fuscicollis weddelli) and interactions with marmosets (Callithrix emiliae)

We present data on aspects of the behavioral ecology of a free- ranging group of Saguinus fuscicollis weddelliat a site in Brazilian Amazonia where a second callitrichid, Callithrix emiliae,is syntopic. Diet, activity patterns, and ranging behavior are broadly similar to those of S. fuscicollisfrom sites in Bolivia, Brazil, and Perú, though significant seasonal changes include an extreme and atypical form of ranging behavior in which they foraged in central-place fashion around a source of exudate—Parkia pendula. S. f. weddelliwas active at relatively low levels in the forest both in absolute terms and relative to C.emiliae, which appears to be an important factor in their niche partitioning. Association between the two species appeared to be less systematic overall than those observed between S. fuscicollisand congeners at other sites, though this may be partly a result of observation conditions. During the period of central-place foraging, the two species exhibited a high degree of association. Other characteristics of the behavior of S. f. weddelliat the study site include the frequent use of tree holes as sleeping sites.     

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.     

The stimulatory effect of males on the initiation but not the maintenance of ovarian cycling in cotton-top tamarins (Saguinus oedipus)

Prior studies have shown that female cotton-top tamarins usually do not ovulate while living with natal groups, and most females do not ovulate until they are paired with an unfamiliar adult male. To examine the role of unfamiliar adult males on stimulating ovarian function, four cotton-top females were studied during three conditions: females living with their natal group for six weeks, living alone but exposed to a single unfamiliar adult male located 15 cm away from the female's cage for four weeks, and living with an unfamiliar adult male for six weeks. Behavior and urinary hormonal concentrations were measured during the three conditions. Exposure to the male consisted of visual, auditory, and airborne olfactory contact. First ovulation occurred during exposure to the unfamiliar male in three of the four females indicating that direct physical or sexual contact with the male is not required for onset of ovarian cycling. The fourth female did not ovulate even during six weeks of direct contact with the unfamiliar adult male. In addition, four parous females in either family groups (3) or singly caged (1) were examined for ovarian function 4–6 months after the death or removal of their mates. All femals continued to cycle in the absence of the male indicating that the male was not needed to continue ovarian cycling. In fact, two of the females were pregnant at the time their males died and both delivered normal infants and resumed cycling. The results of this study indicate that an unfamiliar adult male may facilitate the onset of ovarian cycling without being in direct contact with the female and visual, auditory, or airborne olfactory cues may be involved. Once repeated ovarian cycling occurs the male is not required to maintain ovarian function.     

Genetic influences on cranial form: variation among ranch and feral American mink Mustela vison (Mammalia: Mustelidae)

Multivariate statistical techniques were used to examine craniometric variation within and between ranch and feral populations of American mink (Mustela vison). An examination of variation between ranches revealed that differences are greater between ranches than within ranches, although all comparisons were statistically significant. There is highly significant variation within a population of mink sampled from a single ranch during a short time period; female mink of different pelt colour are differentiable by their skull shape but not by skull size. This offers evidence for a genetic background to cranial variation in ranch mink. Cranial sexual dimorphism is reduced in ranch mink, when compared to feral populations, and size accounts for a lesser proportion of the variation between the sexes in ranched populations. In addition, the skulls of ranched mink are larger, have a relatively shorter palate and a relatively narrower postorbital constriction compared to their feral counterparts. We believe this reduced dimorphism to be a product of relaxed sexual selection, lack of resource competition and selective breeding for larger specimens of both sexes within ranch populations.     

Sexual dimorphism in two subspecies of Ethiopian baboons (Papio hamadryas) and their hybrids

Sexual dimorphism in mammals has been related to such variables as absolute body size, ecology, and various aspects of social behaviour. Attempts to relate dimorphism to any of these variables have necessarily used small heterogeneous samples to represent the relevant species. We are concerned by the inevitable exclusion of any measure of variability in dimorphism and the consequent impossiblity of assessing the significance of observed interspecific differences. In this paper we describe aspects of sexual dimorphism in anubis,hamadryas, and hybrid baboons from Ethiopia. Samples are large enough to permit a measure of intrapopulation variability. Hamadryas baboons are more dimorphic than anubis in epigamic features, but not in postcanine dentition, nor, contrary to previous reports, in body weight or canine tooth size. Hybrid males are more hamadryas-like and hybrid females more anubis-like, as would be predicted by the proposed mechanism for the establishment of the hybrid zone, namely the capture of anubis females by hamadryas males.     

Gummivory and gut morphology in two sympatric callitrichids (Callithrix emiliae and Saguinus fuscicollis weddelli) from western Brazilian Amazonia.

A comparative analysis of the gastrointestinal tracts of wild-caught marmosets, Callithrix emiliae, and tamarins, Saguinus fuscicollis weddelli, was undertaken in order to evaluate the degree of specialisation for digestion of plant exudates. Compared to S.f. weddelli, C. emiliae exhibits a reduced small intestine and a relatively large, compartmentalised caecum in which gum is probably fermented. The apparent specialisation of the digestive tract in C. emiliae correlates with that of its dentition, which is adapted for gouging the bark of gum-producing plants. A similar degree of specialisation of the caecum is predicted for other marmosets (Callithrix spp. and Cebuella pygmaea).     

Effects of prepubertal ovariectomy on the development of scent glands, scent marking, and aggressive behaviors of female tamarin monkeys (Saguinus fuscicollis)

The effects of prepubertal ovariectomy on scent gland development, scent marking behavior, and on social interactions with strange adult conspecifics were studied in adult females cohabiting with intact males. Eight females were ovariectomized and eight underwent control surgery at 6 months of age. All were returned to their families after surgery and allowed to reach sexual maturity. At 18 months of age, each female was permanently paired with an adult, intact male. When the subjects were 21 months old, the social interactions of all pairs with strange adults were tested in a situation analogous to a territorial encounter. The scent marking activities of the subjects and their mates were studied during “territorial encounters,” in trial-free control situations, and in the presence of novel objects. Ovariectomy prior to puberty retarded the development of the scent gland but did not inhibit it completely. Social interactions with strange conspecifics were also affected. Ovariectomized females showed fewer threat displays than did control females, but there was no significant difference in the amount of injurious aggression both female groups directed at the strangers. Under all testing conditions, ovariectomized females tended to scent mark less frequently with the circumgenital-suprapubic gland than did controls. This difference was statistically significant only under some of the testing conditions. Intact females scent marked more frequently than their males but ovariectomized females did so only under trial-free testing conditions. The sternal scent gland was used very infrequently by all subjects and there was no difference in marking activity between males and females or between ovariectomized and control females.     

Proteins: biologically relevant components of the scent marks of a primate (Saguinus fuscicollis)

We report here the first documentation that proteins contributeto the scent communication system in a primate. Data presentedhere indicate that high molecular weight compounds which arenot airborne are required for perception of the full attractivenessof the scent. Scent marks from the saddle-back tamarin, a SouthAmerican primate, contain a number of water-soluble proteins.Gel electrophoresis documents that the major protein (66 kD)is found in urine, and a second protein (18 kD) comes from thegland secretions. The 18 kD protein produces two distinct bands(14 kD and 4 kD) under reducing conditions. Concurrent behavioralstudies demonstrate that removal of proteins by enzymatic degradationdoes not alter the ability of the tamarins to discriminate betweenscents from different donor types. However, subtle changes insensory quality occur when the proteins have been degraded.In particular, tamarins do discriminate material in which theproteins have been digested from material in which the proteinsare intact. This observation suggests that proteins are a componentof what constitutes the scent image. In addition, they may serveas carriers and/or reservoirs for more volatile ligands thatencode some of the communicatory messages contained in the material.     

Bilateral giant myelolipoma in the adrenal of a cotton-top tamarin (Saguinus oedipus)

Abstract: A rare case of bilateral adrenal myelolipomas in a female cotton-top tamarin is reported. Large bilateral masses in the adrenal glands were composed of mature adipose cells containing varying amounts of hematopoietic cells of the myeloid, erythroid, and megakaryocyte series. The gross and histologic features of this case closely resemble human “giant” adrenal myelolipomas.