Responsiveness of expectant male cotton-top tamarins, Saguinus oedipus, to mate's pregnancy

In the cotton-top tamarin, a primate where paternal care is critical to the survival of the offspring, we found that expectant fathers experienced multiple hormonal changes during their mate's pregnancy. Fathers that had experienced several previous births showed significant changes in urinary estrogens, androgens, prolactin and cortisol in the last 2 months before birth, whereas less-experienced fathers (LEF) did not. The female's midpregnancy rise in glucocorticoids was followed within 1-2 weeks by a peak of cortisol and corticosterone in her paired male in 70% of all males and 100% of all experienced males. Examination of behavioral interactions between the pairs did not reveal changes in rates of interactions between the experienced pairs over pregnancy. However, the less-experienced pairs had significantly higher levels of affiliative and sexual interactions. Therefore, behavioral communication between the pair did not appear to account for the hormonal changes occurring within the experienced fathers (EF). The midpregnancy rise of glucocorticoids in females may stimulate a glucocorticoid response in male tamarins and thereby activate other hormonal changes in males to prepare them for their parenting role.     

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.     

Visual encounters between families of cotton-top tamarins,Saguinus oedipus

Territorial, cooperatively-breeding, incest-avoiding organisms have various options for securing mates and resources for breeding. Both philopatry and dispersal have many costs and benefits, but all are likely to include assessment of neighbours. Five families of cotton-top tamarins,Saguinus oedipus, in a laboratory colony were allowed to watch each other through a peephole. These encounters took place in a naturalistic, neutral zone outwith their home room or cage. Parents looked more at neighbours than did offspring. Older monkeys looked more than younger. Females looked more than males. The clearest effect was ofseniority: eldest offspring regardless of age were more eager lookers than were second-eldest than were third-eldest. The results make sense in terms of the monitoring of potential candidates for mate-recruitment or resource-acquisition, or for defense against outsiders with the same interests.     

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.     

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%.     

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.     

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.     

Changes in body mass of expectant male cotton-top tamarins (Saguinus oedipus)

It has been noted that expectant cotton-top tamarin males in captivity experience a body mass increase during the last months of their mates' pregnancies, and this has been explained as being a male physiological response. We studied the body mass of 4 inexperienced and 4 experienced expectant males, and we expected to observe a larger body mass increase among the experienced ones since they undergo multiple hormonal changes in comparison to inexperienced expectant males. However, while inexperienced expectant males gained body mass during months 4-6 of the pregnancy period by a mean +/-SD of 5.4 +/- 3.1% (i.e. 29 +/- 17 g), the experienced ones did not (mean +/- SD of months 4-6, 0.5 +/- 1.7%, i.e. 5 +/- 12 g). The results suggest that other factors, such as behavioural communication between pairs and feeding and resting behaviour, should be studied in order to clarify the basis of this body mass increase.     

Problem solving and functional design features: experiments on cotton-top tamarins, Saguinus oedipus oedipus

In any problem-solving situation, there are features associated with the problem that are relevant from a functional perspective and other features that are irrelevant. To determine whether animals are sensitive to the distinction between functionally relevant and irrelvant features of a problem, we conducted two main experiments with a New World monkey, the cotton-top tamarin. In the first condition of both experiments, subjects were required to pull a piece of cloth to gain access to a piece of food. The first experiment involved choosing between food that was on the cloth and food that was off the cloth. The second experiment involved choosing between food that was on a connected piece of cloth and food that was on two pieces of cloth separated by a horizontal gap. Having learned to solve either of these two problems, we conducted a series of probe conditions to determine whether the tamarins would generalize to changes in the shape, size, colour, and texture of the cloth and food, the position of the food relative to the cloth, and the type of connection between two pieces of cloth. For most of the probe conditions, the tamarins readily generalized, showing no decrement in performance, even on the first trial. For other conditions, involving apparently more subtle discrimination (e.g. a narrow vertical gap between the two pieces of cloth), explicit training was required. These results indicate that tamarins solve means-end relationships, and that their ability depends on a discrimination between properties that are functionally relevant as opposed to irrelevant. Copyright 1999 The Association for the Study of Animal Behaviour.     

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.     

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.     

Developmental changes in food transfers in cotton-top tamarins (Saguinus oedipus)

We investigated the development of food transfer and independent feeding in cotton-top tamarin (Saguinus oedipus) families. We studied the relationship between infant-directed vocalizations and food transfers on the development of independent feeding in infants. We experimentally tested ten infants (eight twins and two singletons) three times a week for 17 weeks from before weaning through 20 weeks. Food transfers and vocalizations made during tests were recorded and analyzed to determine (1) the role of vocalizations (C- and D- chirps and D-chirp series) in food acquisition, (2) the relationship between food transfers and individual food acquisition, and (3) whether, owing to energetic costs of nursing and carrying twins, food is transferred to twins sooner than to singletons. Infants were more successful in acquiring food via begging when adults produced repeated vocalizations than when adults did not vocalize. Adults emitted more food-related vocalizations in rapid series when in the presence of infants, whereas during feeding in the absence of infants only single unit vocalizations were produced. Begging occurred frequently. Changes over infant age were not significant when all infants were included in analysis. However, when twin data were analyzed alone, begging success changed significantly over months, with successful begging peaking in month 3 (week 12). Begging success rate did not differ between twins and singletons, although twins fed independently sooner and at a higher rate than did singletons.     

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.     

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.     

A two-choice preference assessment with five cotton-top tamarins (Saguinus oedipus)

A study selected 5 cotton-top tamarins (Saguinus oedipus) located at the Frank Buck Zoo in Gainesville, Texas, for a food preference assessment. The study used a paired-choice procedure across 7 different food items for all 5 tamarins. Preferences for the food items across all the tamarins varied, although general trends were noted as well. This article discusses the benefits of using paired-choice preference assessments in zoo settings.     

Reproductive events of wild cotton-top tamarins (Saguinus oedipus) in Colombia

Reproductive patterns of wild cotton-top tamarin (Saguinus oedipus) females located in La Reserva Forestal Protectora Serranía de Coraza-Montes de María in Colosó, Colombia, were examined using long-term behavioral observations and fecal steroid analysis. Using an enzyme immunoassay, we analyzed fecal samples for E₁C and PdG. Comparisons of reproductive cycles of a reproductively active female and her daughters were made. An inhibition of ovarian cycles has been observed in daughters living in their families. However, daughters also exhibited normal ovarian cycling that subsequently resulted in pregnancy. Factors influencing the fertility are discussed as they relate to the reproductive strategies of wild cotton-top tamarin females. Am. J. Primatol. 43:329–337, 1997. © 1997 Wiley-Liss, Inc.     

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.     

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.     

Sociosexual development,pair bond formation,and mechanisms of fertility suppression in female cotton-top tamarins (Saguinus oedipus oedipus)

The effect of various social environments on sociosexual behavior was examined in six young female cotton-top tamarins (Saguinus oedipus oedipus) and in three established breeding females. Behavioral observations and hormonal samples were collected on young females while they were living with their families, when they were isolated from conspecifics, and after they were paired with an unrelated male. While living with the family, all females showed a suppression of fertility and low frequencies of sociosexual behavior. Following removal from the family, isolated females displayed an increase in rate of scent marking and an increase in hormonal levels. When young females were paired with males, they were exposed to scent secretions from their natal families, from an unfamilar family, and from a control for a total of 24 weeks. After pairing, hormonal levels increased dramatically, and ovarian cyclicity began. An increase in sociosexual behavior and elevated levels of scent marking accompanied this physiological change. Newly paired females had higher rates of affiliative behavior and scent marking than did established breeding females. However, both newly paired and established breeding males were more likely to initiate contact, grooming bouts, and social sniffing than were females. Time to first ovulation was later in females who were exposed to scent secretions from their natal families than it was in those females given a control for the first 8 weeks following pairing. No female conceived during exposure to scent secretions. However, once normal ovarian cycling had begun or a pregnancy was established, exposure to scent secretions had no effect. Thus, the social environment influences the fertility, sociosexual behavior, and pair bond formation of cotton-top tamarins. In addition, chemical stimuli found in the scent secretions produced by the natal family are most likely involved in reproductive suppression.