The impacts of seasonal variation and climate on food utilization in a population of critically endangered cotton-top tamarins (Saguinus oedipus) in Colombia: A 22-year longitudinal study.

To examine how precipitation patterns and climate change impact feeding choices made by a population of critically endangered cotton-top tamarins (Saguinus oedipus), we examined 22 years of feeding data (1999-2020) from 21 groups collected at Parque Natural Regional Bosque Seco El Ceibal Mono Tití in Santa Catalina, Colombia. We describe the diet and examine the role of seasonal rainfall and annual variation in rainfall on diet. Rainfall is highly seasonal (mean annual rainfall 1562 mm [range 940-2680 mm]) with a dry, early rainy, and late rainy season in each year. Over 80 species of plants formed part of the fruit, nectar, and exudate components of the diet. Fruits, although available year-round, were more commonly available and consumed during the late rainy seasons (August-November). Exudates were consumed more frequently in the dry season (December-March) and invertebrate consumption was stable across the year. Nectar feeding from a single species (Combretum fruticosum) peaked in November. Rainfall varied over the years, with 13 years exceeding the 99% confidence intervals for mean rainfall. Ten of these extreme years (both drought and extremely wet) occurred in the last 11 years. Fruit consumption did not vary between extreme and average years, but cotton-top tamarins consumed more invertebrates and exudates in wet years. Presently, cotton-top tamarins appear to be able to cope with these extreme variations in rainfall due to their highly varied diet. However, the forests that these primates depend upon for survival are threatened by human exploitation making it critically important to maintain a generalist feeding strategy for survival as many fruiting trees that compose a large proportion of the diet are removed. As conservation efforts continue, plant species consumed by cotton-top tamarins provide useful data when selecting species for habitat restoration programs.

Male parenting and response to infant stimuli in the common marmoset (Callithrix jacchus).

Callithrix jacchus infants are raised in complex family environments where most members participate in rearing the young. Many studies examining male parental behavior have focused on the carrying of infants with observations made within the family context. However, interference from family members can make it difficult to assess the father's motivation to care for infants. Our goals were to develop a testing paradigm for determining an individual's response to infant stimuli separate from family influences, compare a male's motivation to respond to an infant stimulus outside the family with his paternal behavior within the family, to compare responses to infant stimuli of parentally experienced versus inexperienced males and finally to develop a reproducible and standardized method of testing male responsiveness to infant stimulus that could serve to evaluate hormonal manipulations. Fifteen experienced common marmoset fathers were evaluated using three different measures of parental behavior: (1) instantaneous scan sampling, (2) continuous focal sampling in the family, and (3) continuous focal sampling of males presented with four infant stimuli: familiar and unfamiliar infants, familiar and unfamiliar infant vocalizations. Six parentally inexperienced males (non-fathers) served as controls. Males that carried the most in the family were typically the same males that responded most to the infant vocalization tests. Experienced fathers did not differ in their latency to enter the stimulus cage for any of the four infant stimuli response tests while inexperienced males took significantly longer to enter the stimulus cage. In addition, fathers expressed a greater frequency of infant-directed behavior than did the inexperienced males during the unfamiliar infant and unfamiliar vocalization tests. These studies show that experienced male marmosets are highly motivated to interact with infant stimuli and that there is interindividual variability in response to infant vocalizations. Testing males outside of the family allows for a clear assessment of male's interest in infant stimuli in both parentally experienced fathers and inexperienced males.

Fruit availability, chimpanzee diet, and grouping patterns on Rubondo Island, Tanzania.

We examined seasonal patterns of fruit availability, dietary quality, and group size in the descendants of an introduced chimpanzee population on Rubondo Island, Tanzania. The site has supported a free-ranging population without provisioning for 40 years. Our goals were to determine whether Rubondo chimpanzees experience periods of fruit shortage, and whether they respond to changes in fruit availability similarly to chimpanzees at endemic sites. We indexed the fruit availability of tree and liana species on transects stratified across three chimpanzee ranging areas. We used fecal analyses to evaluate seasonal changes in diet, and used data on party size and nesting group size to examine seasonal patterns of grouping. Tree fruit availability was positively correlated with rainfall, with a period of relative tree fruit scarcity corresponding with the long dry season. Liana fruit availability was not related to rainfall, and lianas exhibited less variable fruiting patterns across seasons. Fruits made up the majority of the chimpanzee diet, with lianas accounting for 35% of dietary fruit species. Fruits of the liana Saba comorensis were available during all months of phenological monitoring, but they were consumed more when tree fruit was scarce, suggesting that Saba comorensis fruits may be a fallback food for Rubondo chimpanzees. There were no increases in consumption of lower-quality plant parts between seasons, and there were no changes in group size between seasons. These results contrast with evidence from several endemic chimpanzee study sites, and indicate that Rubondo chimpanzees may have access to abundant and high-quality foods year round.

Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates.

Among primate species there is pronounced variation in the relationship between social status and measures of stress physiology. An informal meta-analysis was designed to investigate the basis of this diversity across different primate societies. Species were included only if a substantial amount of published information was available regarding both social behavior and rank-related differences in stress physiology. Four Old World and three New World species met these criteria, including societies varying from small-group, singular cooperative breeders (common marmoset and cotton top tamarin) to large-troop, multi-male, multi-female polygynous mating systems (rhesus, cynomolgus, talapoin, squirrel monkeys, and olive baboon). A questionnaire was formulated to obtain information necessary to characterize the stress milieu for individuals in particular primate societies. We standardized cortisol values within each species by calculating the ratio of basal cortisol concentrations of subordinates to those of dominants in stable dominance hierarchies and expressing the ratio as a percentage (relative cortisol levels). The meta-analysis identified two variables that significantly predicted relative cortisol levels: subordinates exhibited higher relative cortisol levels when they (1). were subjected to higher rates of stressors, and (2). experienced decreased opportunities for social (including close kin) support. These findings have important implications for understanding the different physiological consequences of dominant and subordinate social status across primate societies and how social rank may differ in its behavioral and physiological manifestations among primate societies.

Functional imaging of brain activity in conscious monkeys responding to sexually arousing cues.

Olfactory cues can elicit intense emotional responses. This study used fMRI in male common marmoset monkeys to identify brain areas associated with sexual arousal in response to odors of ovulating female monkeys. Under light anesthesia, monkeys were secured in a specially designed restrainer and positioned in a 9.4 T magnetic resonance spectrometer. When fully conscious, they were presented with the scents of both ovariectomized and ovulating monkeys. The sexually arousing odors of the ovulating monkeys enhanced signal intensity in the preoptic area and anterior hypothalamus compared to the odors of ovariectomized monkeys. These data corroborate previous findings in monkeys based on invasive electrical lesion and stimulation techniques and demonstrate the feasibility of using non-invasive functional imaging on fully conscious common marmosets to study cue-elicited emotional responses.

Social processes in communication and cognition in callitrichid monkeys: a review.

Studies of vocal development in nonhuman primates have found little evidence for plasticity in vocal production, somewhat more for usage of calls, with the greatest plasticity arising in response to calls of others. Generally, similar results were obtained with callitrichid monkeys, the marmosets and tamarins, but with several interesting exceptions. Infant pygmy marmosets show babbling behavior with improvement in adult call structure related to the amount and diversity of babbling. Adult marmosets alter call structure in response to changes in social partners, and wild marmosets have vocal dialects and modify call structure according to how far they are from other group members, suggesting the potential to modify call structure in different social and environmental contexts, though direct learning of novel vocalizations has not been observed. Infant cotton-top tamarins do not produce adult-like calls in appropriate contexts, at least in the first few months of life, but through food sharing from adults infants learn about appropriate foods and the appropriate contexts for food vocalizations. Tamarins modify call structure and usage with changes in social status. Tamarins, unlike other monkeys tested, can learn to avoid noxious foods through observation of other group members, and can learn about novel food locations. Recent studies provide evidence of contextual imitation in marmosets. The plasticity in vocal communication and evidence of social learning in marmosets and tamarins relative to other monkeys may be related to the cooperative breeding system of marmosets and tamarins. With a high degree of behavioral coordination among group members, there is a priority on monitoring signals and behavior of others and adjusting one's own signals and behavior. This creates the context for vocal plasticity and social learning.

Preparental hormone levels and parenting experience in male cotton-top tamarins, Saguinus oedipus.

Male cotton-top tamarins, Saguinus oedipus, display hormonal changes associated with parenting prior to the birth of their infants. Here we examined the hormonal changes that occurred in experienced and inexperienced fathers during the postconception period, prior to the birth of infants. Noninvasive techniques were used to collect urine from 10 male cotton-top tamarins (5 experienced and 5 inexperienced breeders) three times weekly during the 6-month gestation period. Samples were analyzed for prolactin, testosterone, dihydrotestosterone (DHT), and cortisol, averaged by gestational month. Experienced males showed elevated prolactin during the mate's 3rd gestational month, and the elevation correlated with the number of infants surviving from the previous birth (0, 1, and 2) but not with outcome of the current pregnancy. However, an experienced male with no infants present still showed elevated prolactin and some inexperienced males showed elevated prolactin just before parturition, suggesting noninfant cues are also important. While prolactin levels were influenced by the male's prior infant experience, testosterone levels did not differ between experienced and inexperienced males. Testosterone levels were significantly elevated for all males during the 3rd, 4th and 5th months but had no relationship with number of infants present or with outcome of current pregnancy. DHT decreased during the second half of pregnancy compared with testosterone but this finding was not consistent for every male. No significant changes occurred in cortisol levels. These results suggest that infant-rearing experience affected the hormonal responsitivty of the male to his mate's current pregnancy.

Prolactin levels during the periparturitional period in the biparental cotton-top tamarin (Saguinus oedipus): interactions with gender, androgen levels, and parenting.

Unlike biparental bird and rodent species, mating and parenting occur simultaneously in cotton-top tamarins, Saguinus oedipus, providing a unique model for examining endocrine interactions. This study was designed to determine the relationship of prolactin to testicular androgens during parenting and mating. Specifically we examined (1) the patterns of postpartum prolactin excretion in male and female tamarins with and without infant survival; (2) the relationship between androgen and prolactin levels during the periparturitional period in male tamarins; and (3) male hormonal response to the postpartum mating that occurs simultaneously with paternal care. All females showed an elevation in prolactin during the first week postpartum and when infants died, female prolactin levels decreased significantly. Infant survival during the first 15 days did not influence male levels of prolactin, cortisol, or the testicular androgens testosterone and dihydrotestosterone (DHT). Prolactin did not show an inverse relationship with any of the androgens (testosterone, DHT) studied during the postpartum period. No significant differences in hormones were found between prepartum levels and the first, second, and third 5-day blocks postpartum for all 10 males. Males who had infant-care experience showed an increase in testosterone during the first 5 days postpartum and prolactin levels correlated with the number of previous births a male had experienced. However, the most significant changes in testosterone occurred in males whose mates ovulated during the first 15 days following birth in contrast to males whose mates ovulated later than 15 days. These results indicate that unlike females, male tamarins are not showing hormonal changes in response to infants. Urinary androgens did not show an inverse relationship to prolactin in male tamarins, but were elevated concurrent with the female's fertile period.

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.

Gonadal source of testosterone metabolites in urine of male cotton-top tamarin monkeys (Saguinus oedipus).

Examining gonadal function in the small excitable cotton-top tamarin monkey (Saguinus oedipus) requires noninvasive sampling techniques. Two studies were performed to identify the quantifiable urinary metabolites of testosterone in cotton-top tamarins and which of the measurable metabolites would best reflect a gonadal source of testosterone secretion. In the first study, we injected unlabeled testosterone i.m. in males at either 500-ng or 1-microg levels. Urine samples were analyzed for androgens and estrogens. Testosterone and dihydrotestosterone (DHT) increased significantly following the injections in test males but not in control males. No significant increases in androstenedione occurred. Mean levels of estradiol and estrone did not consistently increase during the 5 days following injection. In the second study, a gonadotropin-releasing hormone antagonist, Antide, was used to block LH stimulation of gonadal steroidogenesis. Males given Antide at either a 6 mg/kg dose or an 18 mg/kg dose showed significantly lower levels of urinary LH than controls. At the higher Antide dose, testosterone levels were significantly reduced during weeks 1 and 2 posttreatment, whereas DHT levels significantly declined during the 2nd week posttreatment. Estradiol levels were highly variable prior to treatment but decreased significantly following treatment, whereas estrone levels remained variable throughout. These results indicate that measurement of urinary testosterone and possibly DHT reflect gonadal function in male cotton-top tamarins. Other sources of urinary estrogens may occur for the male cotton-top tamarin, but these data suggest that a substantial part of urinary estradiol is from gonadal sources, whereas urinary estrone appears to be mainly from extragonadal sources.

Chemical communication of reproductive status in female cotton-top tamarins (Saguinus oedipus oedipus).

Among Callitrichids, scent secretions have been identified as carrying information regarding species, subspecies, gender, social status, individuality, hormonal status, and timing of ovulation. We propose that information regarding familiarity and reproductive status is also communicated. Seven male-female pairs of cotton-top tamarins (Saguinus oedipus oedipus) were presented with several drops of distilled water, a scent secretion from the female of that pair, scent secretions from unfamiliar, reproductively mature but noncycling females, and scent secretions from unfamiliar, reproductively cycling females. Behavioral responses from both males and females were recorded over a 10 min period. Differences in behavioral response for both males and females were significant across all four conditions. This indicates that cotton-top tamarins are capable of discriminating a familiar scent from an unfamiliar scent as well as the reproductive status of an unfamiliar female. The communication of this information may play an important role in regulating mate selection, reducing reproductive competition, and stabilizing transfers in and out of groups in the wild.

`Babbling' and social context in infant monkeys: parallels to human infants.

Although only humans use spoken language, the vocal communication of many animals shares some features with language. Within the context of their family, normal children and young non-human primates develop proficiency in the nuances of their species-specific vocal communication system. Engaging in speech-like phonetic activity, or babbling, occurs in all normal children regardless of their native language. Similar periods of vocal development have not been described previously for non-human primates. However, in the pygmy marmoset, a South American monkey, we found that the primary vocal behavior of infants parallels many characteristics of human infant babbling. These analogous features include universality, repetition, use of a subset of the adult vocal repertoire, recognizably adult-like vocal structure and lack of a clear vocal referent. Also, like human infants, young marmosets develop in a closely knit family unit that includes both parents and often older siblings. In this context, the babbling-like behavior of the marmoset infant stimulates interaction with caregivers, thereby serving a key role in the infant's own development. These developmental and social processes indicate that the study of vocal development in non-human primate species can provide insights into the function of babbling in humans.

Affiliative processes and vocal development.

Affiliative behavior is often expressed through communication, and the nature of affiliative interactions affects the ontogeny of communication. I presented three phenomena that demonstrate the importance of affiliation in vocal development in marmosets and tamarins, but the results have parallels in many other species including birds, dolphins, and humans. Pygmy marmosets use trill-like vocalizations to maintain contact with other group members. Individuals change subtle aspects of call structure when they encounter new social groups or acquire a new mate. This process of vocal accommodation is common in many other species. Infant pygmy marmosets go through a stage of "babbling." producing long sequences of vocalizations that have several similarities to the babbling of human infants. Babbling infants receive more social attention than nonbabbling infants, and these social interactions may shape vocalizations towards more adult forms. In adult cotton-top tamarins, food-associated vocalizations communicate the presence and quality of food. However, reproductively inhibited juveniles and subadults use many other types of calls in feeding situations and display a high proportion of imperfect forms of adult food-associated calls. When subadult monkeys are paired with new mates and change their reproductive status, they rapidly (within 3-6 weeks) display both adult structure and adult usage of food-associated calls, suggesting that affiliative processes can both facilitate and inhibit vocal ontogeny. Three mechanisms of how social interactions affect communication (multimodal stimulation, attentional focus, and reinforcement) were proposed and illustrated through examples of parrots learning English labels for objects and attributes and infant cotton-top tamarins acquiring food-associated vocalizations.

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.

Ovarian function of pygmy marmoset daughters (Cebuella pygmaea) in intact and motherless families.

Reproductive inhibition of subordinate Callitrichid group members has been shown to vary with genus; whereas female Leontopithecus subordinates have normal ovarian cycles and occasionally breed within groups, subordinate Saguinus females almost never do so, with Callithrix species showing intermediate levels of reproductive inhibition. No information has been available on patterns of reproduction or inhibition in subordinate females in the genus Cebuella. We assessed fertility in Cebuella pygmaea daughters to allow comparison with the remaining Callitrichid genera. Specifically, the project had two goals: 1) to determine if there was evidence of reproductive inhibition of daughters living in family groups, and 2) to compare the ovarian function of daughters living in intact family groups with that of daughters residing in motherless families (i.e., without the breeding female). We collected daily urine samples for 6-8 weeks from eight pygmy marmoset daughters living in intact family groups or motherless families. Determination of ovulatory cycling or reproductive quiescence depended on the hormonal profiles generated from urinary luteinizing hormone and pregnanediol-3-glucuronide concentrations. All females in the motherless condition (aged 13-30 months) (n = 4) ovulated during the study. In contrast, only one of four daughters (aged 13-20 months) residing in intact families was found to be cycling. Data from motherless groups indicate ovarian cycling may begin between 15 and 17 months of age. Reproductive inhibition occurs in pygmy marmosets, although in a pattern more similar to Callithrix than to other Callitrichid genera.

Hormonal responses to parental and nonparental conditions in male cotton-top tamarins, Saguinus oedipus, a New World primate.

The socially monogamous cotton-top tamarin (Saguinus oedipus) monkey is a cooperative breeder with the breeding male providing extensive parental care shortly after birth. We examined the relationship of urinary prolactin and cortisol excretion both to male parental care and as a stress response in the cotton-top tamarin monkey. First-morning urine samples were collected to determine hormonal concentrations. Hormonal and behavioral data were collected on 8 male cotton-top tamarins during the 2 weeks before and the 2 weeks following birth of infants to their mate, 11 nonparental males with exposure to females, and three eldest sons from large family groups. Prolactin levels were significantly higher in experienced fathers during the postpartum period than in the other males, while cortisol levels were significantly lower in experienced fathers and eldest sons. Prolactin levels in experienced fathers were consistently elevated before birth, following birth, and after infants were weaned; prolactin levels during times of infant independence were still significantly higher than those in nonfather males. First-time fathers exhibited prolactin levels that were significantly higher after the births of infants than these same males did when they were paired with nonpregnant females. Elevated prolactin concentrations also occurred prior to the first birth, suggesting that males may be receiving cues from their pregnant females. The elevated prolactin levels in parental males may be associated with the experience of the fathers. Correlation between prolactin levels and number of successful births, number of previous births, and age were high. The care of newborn infants did not appear to be a stressful event since cortisol levels were not elevated postpartum. Both cortisol and prolactin were elevated following capture and injection of saline or a dopaminergic receptor antagonist, indicating that prolactin does respond to acute stress. Cortisol levels did not coincide with prolactin levels except under acute stress conditions, suggesting that different neural pathways are probably involved in prolactin release during parental care versus acute stress. These studies provide evidence that male urinary prolactin levels may be elevated due to cues from pregnant females and the constant exposure of males to the family environment.

Metabolism of reproductive steroids during the ovarian cycle in two species of callitrichids, Saguinus oedipus and Callithrix jacchus, and estimation of the ovulatory period from fecal steroids.

Gonadal steroids were measured in daily fecal samples providing comparative data on steroid metabolism in two genera of New World primates. Circulating bioactive LH and progesterone concentrations and fecal progesterone, pregnanediol, estradiol, and estrone concentrations were measured by collecting blood and daily fecal samples from four captive common marmoset females and four cotton-top tamarin females for 30 days. High recoveries (> 80%) of labeled steroids that were added directly to the feces before extraction were recovered from feces of both species. Because of the presence of complex steroid conjugates, only one fifth the amount of estradiol was measured without solvolysis as compared to the amount measured with solvolysis. In tamarins, steroids were metabolized rapidly, with all postovulatory increases occurring within two days after the circulating LH peak (an increase of 2 SD higher than mean follicular levels). In marmosets, steroid excretion was slower; increased steroid levels occurred 2-4 days after the LH peak except in the case of estrone, which did not consistently increase after the LH peak. Circulating estrone and estradiol both contributed to the high excretion of estradiol in the feces from both species. The timing in the delay in excretion of fecal steroids was used to accurately determine the ovulatory period to within a 2-day window. This degree of accuracy is possible when the duration of the delay to the LH peak is known for a given species. Additionally, steroid concentrations were highly correlated between frozen and lyophilized fecal samples (0.81 +/- 0.07 SEM), indicating that fluid removal from the feces did not effectively alter steroid profiles.