Causes of mortality in captive cotton‐top tamarins (Saguinus oedipus)

Cotton‐top tamarins have been housed in captivity in the United States for over five decades. These animals initially were managed in biomedical and research facilities, and more recently have been kept in zoos as well. Although the causes of mortality in captive cotton‐top tamarins have been a topic of investigation for biomedical colonies, they have not been addressed for the North American zoo population. In this retrospective study we review the causes of mortality in the AZA Cotton‐top Tamarin Species Survival Plan (SSP)© population during 1997–2001 to assess current husbandry practices and assist in further developing effective husbandry and management programs for this endangered species. Zoo Biol 23:127–137, 2004. © 2004 Wiley‐Liss, Inc.     

Cotton-top tamarins (Saguinus oedipus oedipus): Hematologic reference values and hemopathologic responses

Hematologic reference values have been established for captive adult cotton-top tamarins (Saguinus oedipus oedipus) by carrying out full blood counts and fibrinogen estimation on 43 clinically normal animals. Females were shown to have significantly lower hemoglobin levels, red cell counts and packed cell volumes, and higher reticulocyte counts than males. The reference values were used to identify abnormal changes in the blood of 13 clinical cases. Marked neutrophilia was found in animals with localized bacterial infections, and a degenerative left shift was recorded in an individual with streptococcal septicemia. Three cases of unexplained progressive muscle wasting showed Heinz body anemia and abnormal white cell changes. These hematologic responses have been compared where possible with those recorded in other species of Callithricidae.     

Cotton-top tamarins (Saguinus oedipus) fail to show mirror-guided self-exploration

To investigate the problem of inter- and intraspecific differences on the mirror test, we conducted two experiments on cotton-top tamarins. Experiment 1 employed a technique similar to one used recently on chimpanzees, and provided no evidence of mirror-mediated touching of the marked area. In a control condition, involving colored dye applied to one arm, two subjects also failed to show self-directed touching, even though they clearly looked at their newly dyed arm. Under these test conditions, cotton-top tamarins fail to show mirror-guided self-exploration. Experiment 2 examined whether this failure was due to insufficient mirror exposure, as well as other details of the testing conditions. In particular, we replicated the design of a previously successful experiment on mirror-mediated recognition in tamarins [Hauser et al., 1995], providing four new animals with a protracted period (three weeks) of mirror exposure prior to dying their hair. In parallel with results from Experiment 1, we observed no evidence of mirror-mediated behavior (recognition) in Experiment 2.     

Energy requirements of captive cotton-top tamarins (Saguinus oedipus oedipus)

Food intake of captive cotton-top tamarins was measured at various stages of the life cycle and energy intake was calculated from the results. The intake of adults for maintenance was found to vary around 500 kJ X kg-3/4 X day-1 and to decrease with age. During the last 8 weeks of pregnancy, females increased in weight by about 2 g X day-1 but energy intake did not show a marked rise above the maintenance range. During lactation, their energy intake appeared to double. Measurements of intake at various stages of growth were compared with a model of the energy requirements for growth which predicted intake quite closely. Compared with non-primate mammals of similar size, the growth rate of this species is slow, and because of this, the energy intake during growth and lactation is also comparatively low.     

A breeding colony of cotton-top tamarins (Saguinus oedipus)

A breeding colony of cotton-top tamarins is described where 91% of the breeding females are from the first and second laboratory-born generations, and whose infants have a one year survival rate of 62%. Mortality is greatest in the first week of life, and mortality rate is greater for a female's first litter than for subsequent litters. Females without early experience in caring for other infants have a higher infant mortality rate than females with such experience. No seasonal birth patterns have been observed. Large complex cages with food, water and runways located in the upper half of the cage, high protein diets and reduced handling of animals are suggested as additional variables affecting breeding success.     

Parturition and perinatal behaviour in captive cotton-top tamarins (Saguinus oedipus)

Fourteen births to seven female cotton-top tamarins in a successful breeding colony were observed. All births occurred between 17:50 and 20:40. Behavioural changes indicating the onset of labour are described. Delivery was usually accomplished rapidly, with short intervals between successive infants. One suspected and one verified breech presentation occurred; these deliveries were accompanied by a marked increase in the duration of the interval between infants, and one infant apparently died during expulsion. All other presentations seen were vertex occiput posterior. Fathers, and sometimes older offspring of both sexes, frequently shared with the mother in eating the placenta. Carrying of infants by individuals other than the mother was rare in the hour after birth, and was usually confined to fathers. One primipara rejected her second-born infant, but all other parents showed competent parental behaviour from birth onwards. The results are compared to data from other primates, and their relevance to the successful breeding of this species is discussed.     

Three spontaneous lymphomas in a colony of cotton-top tamarins (Saguinus oedipus)

Cotton-top tamarins are well known for their prevalence to idiopathic colitis and adenocarcinomas. At the same time, information on the incidence of spontaneous lymphomas in this highly endangered species is rare. Records, 212 in total, of cotton-top tamarins (Saguinus oedipus) necropsied at the German Primate Centre between 1979 and 1998 were viewed to establish the prevalence of lymphoid neoplasms. Neoplastic lymphoid cell growth was mentioned in three necropsy records. Immunohistology was performed in all three cases on the remaining formalin-fixed, paraffin-embedded tissue using antibodies against CD20, CD3, lysozyme, Ki-67, IgM, IgG, kappa, lambda and EBNA-2. Combining histological and immunohistological results, the lymphomas could be differentiated into two low-grade T-cell lymphomas and one high-grade multicentric polymorphic B-cell lymphoma. This corresponds to a 1.4% incidence of lymphomas in our cotton-top tamarin population over a period of 19 years. Although frozen material was not available and virological testing could not be carried out, clinical or histological evidence did not support an aetiological role of Herpes (H.) saimiri, H. ateles, simian T-cell leukaemia virus type 1 (STLV-1) or Epstein-Barr-related herpesvirus in any of these cases. The lymphomas were considered to be spontaneous.     

Measurement of scrotum and testis size of unrestrained captive cotton-top tamarins (Saguinus oedipus oedipus)

Reproduction is restricted to a small number of animals within both captive and wild groups of callitrichid monkeys (marmosets and tamarins). Sexual development of nonbreeding group members might differ from that of active breeders. Measurements of physical growth typically involve animal handling. However, capture and restraint of callitrichid monkeys can disrupt natural behaviors and physiology. This study introduces a method for estimating size of external genitalia by measuring frontal scrotum width of unrestrained cotton-top tamarin males. We examined whether scrotum width was a reliable indicator of testis size, and whether the method provided information useful for comparisons of growth and development among individuals. Animals were lured to a standardized position, and maximum width of the scrotum was systematically compared to a card with a series of rectangles graded in 1 mm increments. Card measures were validated with caliper measurements of scrotum width and testicle dimensions. Regressions of testes dimensions measured by caliper on scrotum width measured by card were between 82 and 93%, suggesting that measures of frontal scrotum width provide consistent estimates of relative testis sizes. The period of rapid growth ended by roughly two years of age, after which scrotum size did not differ from that of breeding males.     

Food-sharing in cotton-top tamarins (Saguinus oedipus)

Food-sharing behaviour was observed in 9 captive families of cotton-top tamarins (range 4-14 individuals per group), during meals of fresh fruit. Food was transferred to infants by their parents and older sibs in response to begging, and was also offered to them without prior solicitation. Older, mature, reproductively suppressed individuals shared more than young immature monkeys. Infants in larger families received more food than those in smaller ones, though individuals in smaller families shared more. Transfer to infants increased to a maximum at 12 weeks of age and then declined gradually. At one year of age they no longer received food from others. Food sharing by older siblings is a form of helping behaviour which may increase their inclusive fitness, and benefit parents, both directly, by reducing the costs they incur in rearing young, and indirectly, by increasing the amount of food available to infants.     

Adrenal gland tumours in two cotton-top tamarins (Saguinus oedipus oedipus)

Two adrenal gland tumours in captive born cotton-top tamarins (Saguinus oedipus oedipus) are described. One was a pheochromocytoma in a 14-year-old male, the other one a cortical adenoma in a 7.5-year-old female. Both were associated with morphological signs of myocardial damage and circulatory problems. The findings are discussed and compared to adrenal gland tumours in man.     

The effect of the captive environment on activity of captive cotton-top tamarins (Saguinus oedipus)

This study examined captive cotton-top tamarin (Saguinus oedipus) behavior across 3 different exhibits: (a) a rainforest (30.5 m in diameter), where tamarins free-ranged with other species; (b) a caged outdoor exhibit (5 m in diameter); and (c) a caged enclosure, with access indoors (6 × 9m) and outdoors (2.5 × 2.5 m). The study observed tamarins using focal animal scan sampling in 10 min blocks. Scoring was on the percentage of intervals in which they engaged in 12 behaviors. The findings show significant differences in activity, inactivity, and visibility across exhibits and have important implications for reintroduction efforts.     

Factors in the rejection and survival of captive cotton top tamarins (Saguinus oedipus)

Captive colonies of cotton top tamarins experience a high rate of rejection of infants within the 1st week of life. The rates of rejection and survival to maturity (2 or more years) among 659 live colony-born infants were correlated with rearing, birth group, litter size, season of birth, gender, origin of parents, experience of parents raising siblings, parity and age of parents, and experience of parent pairs. The most important factors associated with low rejection rates were family life and parental experience raising infants. Infants born into family groups or reared in families were rejected at a significantly lower rate. Rejection of infants whose sires were raised with siblings was significantly lower. Paternal experience was more important than maternal experience. Litter size had no effect on rejection of infants born to family groups, whereas, rejection of triplets was significantly higher than twins or singles among those born to parents alone. Rejection was significantly higher among primiparous births than multiparous birth. The combined experience of colony-born parents was not related to rejection if there were no sibling helpers in the cage at the time of birth. Rejection was significantly lower if sibling helpers were present. High survival of infants who were not rejected was correlated with rearing by or being born into family groups and higher parity and older age of the sires.     

Rearing a second generation of cotton-top tamarins (Saguinus oedipus oedipus) in captivity

The average age at first parturition in captive-born female cotton-top tamarins was 31 months. Only 18% of full-term young born were successfully reared by primiparous females, but success increased with parity and 71% of babies born at 4th and 5th pregnancies were raised. 15% of litters were single births, 61% were twins and 24% were triplets. There was a seasonal distribution of births, with a clear peak in the spring months. The average interbirth interval was 294 days.     

Noise-induced vocal modulation in cotton-top tamarins (Saguinus oedipus)

The Lombard effect-an increase in vocalization amplitude in response to an increase in background noise-is observed in a wide variety of animals. We investigated this basic form of vocal control in the cotton-top tamarin (Saguinus oedipus) by measuring the amplitude of a contact call, the combination long call (CLC), while simultaneously varying the background noise level. All subjects showed a significant increase in call amplitude and syllable duration in response to an increase in background noise amplitude. Together with prior results, this study shows that tamarins have greater vocal control in the context of auditory feedback perturbation than previously suspected.     

Reconciliation in captive cotton‐top tamarins (Saguinus oedipus), a cooperative breeding primate

Reconciliation has been demonstrated in all primate species in which the phenomenon has been studied. However, reconciliation has been studied in only two species of callitrichids, and conclusions remain controversial. The first aim of this study has been to find out whether captive cotton‐top tamarins (Saguinus oedipus) reconcile, since this is the first such study on this species. We examined 227 conflicts in three family groups (N=19). Instances in which individuals remained together in t=0 (29; 12.8%) were not analyzed. The cotton‐top tamarins showed heightened affiliation between opponents in the postconflict periods (PC) compared with matched control (MC) periods (39.88±5.12% and 3.18±1.27%, respectively), with a corrected conciliatory tendency of 37.17±5.37%, and a “time window” that included the first 180 sec of the PC period. Former opponents were the most likely recipient of affiliative behaviors during the PC periods: 39.83±4.26% vs. 11.36±5.33% during MC periods. The proportion of attracted pairs (47.13±6.25%) was significantly higher than those of dispersed pairs for male–male conflicts (3.79±1.79), but not for male–female conflicts (27.31±9.32 and 4.82±2.9, respectively). In cooperative‐breeding species, specific sex‐class dyads might differ in how they resolve conflicts. Am. J. Primatol. 71:895–900, 2009. © 2009 Wiley‐Liss, Inc.     

Changes in the activity of captive cotton-top tamarins (Saguinus oedipus) over the breeding cycle

The energetic costs of reproduction are likely to be particularly high in the Callitrichidae (marmosets and tamarins), which characteristically produce twin litters. The activity of five captive breeding pairs of cotton-top tamarins (Saguinus oedipus) was investigated for a 6-month period covering the second half of pregnancy and lactation. Breeding males showed few major changes in activity over this period, but breeding females reduced their levels of locomotion during late pregnancy, and during lactation they spent up to twice as much time feeding and foraging as they did during pregnancy. These results support the hypothesis that the costs that callitrichid females incur when reproducing are likely to have been an important factor in the evolution of these species' communal rearing systems.     

A retrospective study of infant mortality of cotton-top tamarins (Saguinus oedipus) in captive breeding

Fifty of 156 (32%) colony bred cotton-top tamarins were stillborn, and 31 (20%) died within the first week after birth. The stillbirth rate was related to litter size and parity in captivity. A higher percent of single births were stillborn (69%) compared to those of twin births (26%) (p less than 0.005). A higher percent of infants born of the first litter in captivity (42%) were stillborn than those of subsequent litters (23%) (p less than 0.025). Stillbirths were not related to season of birth or sex of infant. Survival of live infants was unrelated to season of birth, sex, litter size, or number of litters.     

Pachyonychia congenita-like disorder in cotton-top tamarins (Saguinus oedipus oedipus).

A spontaneous genodermatosis in 13 cotton-top tamarins is described as a retrospective study. The disease appeared as alopecia, pigmentary disturbances, and claw dystrophy similar but not identical to human Pachyonychia congenita. The disease in the tamarins seems to be inherited as an autosomal recessive trait, becoming clinically apparent around adolescence. In certain families the neonatal mortality rate was also above average, reaching 100%.     

Congenital anomalies in two neonatal tamarins (Saguinus oedipus and Saguinus fuscicollis)

Congenital anomalies were seen at necropsy of two neonatal tamarins. The defects included achondroplastic-like dwarfism, polydactyly and syndactyly in a Saguinus oedipus, and scoliosis and uterus didelphys in a S. fuscicollis. Both infants were the offspring of incestuous matings between twin siblings.     

Observational methods to measure behaviors of captive cotton‐top tamarins (Saguinus oedipus)

The purpose of this study was to identify efficient sampling methods for establishing accurate activity budgets for zoo animals. Seven cotton‐top tamarins (Saguinus oedipus) from two zoos were videotaped for multiple 90 min sessions, 3 to 4 days per week for 12 weeks. An activity budget was constructed for each animal using a continuous sampling method to analyze 30 hr of video recording of each animal. These master datasets, reflecting actual behavior, were re‐sampled using interval sampling lengths of 0.25, 0.5, 1, 2, 4, 5, 7, 10, 15 and 20 min, and cluster sampling protocols (periodic sessions of continuous sampling) of 10 min×3, 15 min×2, 20 min×1, 15 min×1 and 10 min×1 (min×repetitions/90 min sample period) to construct additional activity budgets for each animal. The Canberra similarity index was used to determine the statistical relationship between these activity budgets and those based on the master datasets. As interval length increased, there was a consequent decrease in the accuracy of the associated activity budgets as compared with the master dataset. No cluster sampling protocols yielded activity budgets as accurate as the four shortest interval lengths, but all cluster sampling protocols were more accurate than the three longest interval lengths. All the tested protocols varied in ability to accurately portray animal behavior. Overall, interval sampling provided superior behavioral representations at lower observer input. Results from this study will potentially facilitate the standardization of behavior monitoring protocols at zoos. Zoo Biol 29:416–431, 2010. © 2009 Wiley‐Liss, Inc.