Saguinus Oedipus Research Articles

Comparative lifespan and healthspan of nonhuman primate species common to biomedical research.

There is a critical need to generate age- and sex-specific survival curves to characterize chronological aging consistently across nonhuman primates (NHP) used in biomedical research. Sex-specific Kaplan-Meier survival curves were computed in 12 translational aging models: baboon, bonnet macaque, chimpanzee, common marmoset, coppery titi monkey, cotton-top tamarin, cynomolgus macaque, Japanese macaque, pigtail macaque, rhesus macaque, squirrel monkey, and vervet/African green. After employing strict inclusion criteria, primary results are based on 12,269 NHP that survived to adulthood and died of natural/health-related causes. A secondary analysis was completed for 32,616 NHP that died of any cause. Results show a pattern of reduced male survival among catarrhines (African and Asian primates), especially macaques, but not platyrrhines (Central and South American primates). For many species, median lifespans were lower than previously reported. An important consideration is that these analyses may offer a better reflection of healthspan than lifespan since research NHP are typically euthanized for humane welfare reasons before their natural end of life. This resource represents the most comprehensive characterization of sex-specific lifespan and age-at-death distributions for 12 biomedically relevant species, to date. These results clarify relationships among NHP ages and provide a valuable resource for the aging research community, improving human-NHP age equivalencies, informing investigators of expected survival rates, providing a metric for comparisons in future studies, and contributing to understanding of factors driving lifespan differences within and among species.

TITIRITIANDO: Creating an engaging theatrical education program to teach children that cotton-top tamarins (Saguinus oedipus) are not pets.

Cotton-top tamarins (Saguinus oedipus) are a critically endangered primate found only in Colombia. Proyecto Tití has been leading conservation efforts in Colombia and has developed successful conservation education programs that engage communities in activities that promote the long-term survival of cotton-top tamarins. TITIRITIANDO is an educational theatrical program that introduces children to cotton-top tamarins and the challenges they face in the illegal pet trade. We presented this program to 4018 elementary school children to determine if using puppets and interactive messaging created an emotional connection between children and cotton-top tamarins that inspired them to engage in actions that aid cotton-top tamarin conservation. Pre- and post-test evaluations were conducted on 1917 students. Pre-surveys found 34% of the children were unable to identify at least one action to help cotton-top tamarins. Following the program students could on average identify at least 3 actions that positively impacted cotton-top tamarins with "not having a cotton-top tamarin as a pet" (75%) as the most frequently sited response. Misconceptions regarding the health and wellbeing of pet cotton-top tamarins was evident with 20% of the students believing that animals were well cared for and had a better life living with people than in the forest. Following the program, students were able to understand and empathize with pet cotton-top tamarins and on average could identify at least 3 negative impacts on individual welfare/well-being with the most common answers as they (1) are sad/depressed (91%), (2) die (87%), (3) are fed an inappropriate diet (80%), (4) have lost their family (74%) and (5) have lost their freedom (39%). This study demonstrates the effectiveness of educational theater in helping children to understand the impact the illegal pet trade has on cotton-top tamarins and how they can engage in activities to protect them.

Is inferential reasoning a distinctly human cognitive feature? Testing reasoning in cotton-top tamarins (Saguinus oedipus).

Logical inference is often assumed a human-unique ability, although many species of apes and monkeys have shown some facility within a two-cup task in which one cup is baited, the primate is shown the cup which is empty (an exclusion cue), and subsequently chooses the other baited cup. In published reports, New World monkey species show a limited ability to choose successfully, often with half or more of the subjects tested not showing the ability with auditory cues or with exclusion cues. In this study, five cotton-top tamarins (Saguinus oedipus) were tested in a two-cup task with visual or auditory cues which revealed the presence or absence of bait, and in a second study, were tested with a four-cup array using a variety of walls to define the baiting space and a variety of visual cues including inclusion and exclusion. Tamarins demonstrated the ability to use either visual or auditory exclusion cues to find rewards in the two-cup study, although the visual cue required some exposure before accuracy was expressed. Experiment 2 revealed that two of three tamarins' first guesses to find rewards matched best a logic model. When they made errors, they typically chose cups adjacent to the cued location or made choices that seemed generated from avoiding empty cups. These results suggest that tamarins can deduce the location of food using reasoning, although the ability is only applied robustly to first guesses, while second guesses are motivated by approach/avoidance and proximity to cued locations. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

A recognition test in monkeys to differentiate recollection from familiarity memory

Episodic memory is memory for experiences within a specific temporal and spatial context. Episodic memories decline early in Alzheimer’s Disease (AD). Recollection of episodic memories can fail with both AD and aging, but familiarity and recollection memory uniquely fail in AD. Finding a means to differentiate specific memory failures in animal models is critical for translational research. Four cotton top tamarins participated in an object recognition test. They were exposed to two unique objects placed in a consistent context for 5 daily sessions. Next a delay of 1 day or 1 week was imposed. Subjects’ memory of the objects was tested by replacing one of the familiarized objects with a novel one. The tamarins looked longer at the novel object after both delays, an indication of remembering the familiar object. In other tests, the test pair was relocated to a new location or presented at a different time of day. With context changes, tamarins showed greater interest in the novel object after a 1-week delay but not after a 1-day delay. It seems that context changes disrupted their recollection of recent events. But the monkeys showed accurate familiarity memory across context changes with longer delays.

Efficacy of Edible and Leisure Reinforcers with Domestic Dogs.

Preference assessments are often used to identify stimuli that function as potential reinforcers for training or intervention purposes. Specifically, various preference assessment formats have been used to identify preferred stimuli for humans, cockroaches, cotton-top tamarins, tortoises, and wolves, to name a few. However, to date, no study has evaluated the differential efficacy between food and leisure stimuli within domestic dogs. The current study aimed to compare the reinforcing value and efficacy between food and leisure stimuli for domestic dogs by comparing rates of behavior when receiving access to either their top-preferred food or leisure items. Overall results suggest (1) domestic dogs prefer food over leisure items, and (2) food is more likely to function as a reinforcer than leisure items for domestic dog's behavior. These results suggest that dog owners and trainers should consider using food reinforcers over leisure items as reinforcers when attempting to train dogs.

Effects of Aeriscardovia aeriphila on growth performance, antioxidant functions, immune responses, and gut microbiota in broiler chickens.

Aeriscardovia aeriphila, also known as Bifidobacterium aerophilum, was first isolated from the caecal contents of pigs and the faeces of cotton-top tamarin. Bifidobacterium species play important roles in preventing intestinal infections, decreasing cholesterol levels, and stimulating the immune system. In this study, we isolated a strain of bacteria from the duodenal contents of broiler chickens, which was identified as A. aeriphila, and then evaluated the effects of A. aeriphila on growth performance, antioxidant functions, immune functions, and gut microbiota in commercial broiler chickens. Chickens were orally gavaged with A. aeriphila (1×109 CFU/mL) for 21 d. The results showed that A. aeriphila treatment significantly increased the average daily gain and reduced the feed conversion ratio (P<0.001). The levels of serum growth hormone (GH) and insulin-like growth factor 1 (IGF-1) were significantly increased following A. aeriphila treatment (P<0.05). Blood urea nitrogen and aspartate aminotransferase levels were decreased, whereas glucose and creatinine levels increased as a result of A. aeriphila treatment. Furthermore, the levels of serum antioxidant enzymes, including catalase (P<0.01), superoxide dismutase (P<0.001), and glutathione peroxidase (P<0.05), and total antioxidant capacity (P<0.05) were enhanced following A. aeriphila treatment. A. aeriphila treatment significantly increased the levels of serum immunoglobulin A (IgA) (P<0.05), IgG (P<0.01), IgM (P<0.05), interleukin-1 (IL-1) (P<0.05), IL-4 (P<0.05), and IL-10 (P<0.05). The broiler chickens in the A. aeriphila group had higher secretory IgA (SIgA) levels in the duodenum (P<0.01), jejunum (P<0.001), and cecum (P<0.001) than those in the control group. The messenger RNA (mRNA) relative expression levels of IL-10 (P<0.05) and IL-4 (P<0.001) in the intestinal mucosa of chickens were increased, while nuclear factor-‍κB (NF‍-‍κB) (P<0.001) expression was decreased in the A. aeriphila group compared to the control group. Phylum-level analysis revealed Firmicutes as the main phylum, followed by Bacteroidetes, in both groups. The data also found that Phascolarctobacterium and Barnesiella were increased in A. aeriphila-treated group. In conclusion, oral administration of A. aeriphila could improve the growth performance, serum antioxidant capacity, immune modulation, and gut health of broilers. Our findings may provide important information for the application of A. aeriphila in poultry production.

Assessing the genetic composition of cotton-top tamarins (Saguinus oedipus) before sweeping anthropogenic impact.

During the last century, the critically endangered cotton-top tamarin (Saguinus oedipus) has been threatened by multiple anthropogenic factors that drastically affected their habitat and population size. As the genetic impact of these pressures is largely unknown, this study aimed to establish a genetic baseline with the use of temporal sampling to determine the genetic makeup before detrimental anthropogenic impact. Genomes were resequenced from a combination of historical museum samples and modern wild samples at low-medium coverage, to unravel how the cotton-top tamarin population structure and genomic diversity may have changed during this period. Our data suggest two populations can be differentiated, probably separated historically by the mountain ranges of the Paramillo Massif in Colombia. Although this population structure persists in the current populations, modern samples exhibit genomic signals consistent with recent inbreeding, such as long runs of homozygosity and a reduction in genome-wide heterozygosity especially in the greater northeast population. This loss is likely the consequence of the population reduction following the mass exportation of cotton-top tamarins for biomedical research in the 1960s, coupled with the habitat loss this species continues to experience. However, current populations have not experienced an increase in genetic load. We propose that the historical genetic baseline established in this study can be used to provide insight into alteration in the modern population influenced by a drastic reduction in population size as well as providing background information to be used for future conservation decision-making for the species.

Microplastics Occurrence in Fish from Tocagua Lake, Low Basin Magdalena River, Colombia

Following global trends, research to determine the presence and abundance of microplastics (MPs) in environmental matrices in Colombia has focused on the coastal and marine environments. However, little scientific information is available on the impact of this pollutant on wetlands and fish. In this study, we provided scientific data on the occurrence and abundance of MPs in water and fish from Tocagua Lake, an important wetland in the Colombian Caribbean, and the unique habitat of wild cotton-top tamarins (Saguinus oedipus). Water (72) and fish (228 individuals of six species) samples were collected during four sampling events and two climatic seasons (wet and dry). A total of 1174 microplastic particles were collected in water with an average abundance of microplastics at the six stations sampled during four sampling events of 0.96 ± 0.40 MPs/L, and 648 MPs were identified in the gastrointestinal tract of 191 individuals, corresponding to a frequency of occurrence of 83.7%. Black- and blue-colored fiber MPs were particles that predominated in both matrices (water and fish), and seven types of polymers were identified through attenuated total reflectance Fourier transform infrared spectroscopy analysis. The abundance, type, and color of MPs in water and fish were not significantly different between seasons.

Precursors and aftermath of severe targeted aggression in captive cotton-top tamarins.

We observed a zoo-housed group of cotton-top tamarins (Saguinus oedipus) before and after a bout of severe targeted aggression directed towards two of its members. The aggression was so severe and repeated that the zoo personnel was forced to remove the two victims and the main aggressor. In the tense period that preceded removal, the tamarins showed increased aggression, a steeper and linear dominance hierarchy, and reduced post-conflict reconciliation compared to the period following removal. In contrast, affiliative interactions such as grooming and peaceful food transfers did not differ in the two periods of observations. Patterns of reciprocity also remained stable. These results highlight the flexibility of tamarin social relationships and provide useful information for managing captive colonies and improving animal welfare.

Social Network Changes in Cotton-Top Tamarins (Saguinus oedipus) after the Birth of New Infants.

Cotton-top tamarins (Saguinus oedipus) are characterized by a system of cooperative breeding where helpers, in addition to the reproductive pair, contribute to infant care. Grooming interactions between individuals play an important role in establishing social relationships, creating an interconnected social network in the group. We used social network analysis to investigate the social structure of two groups of cotton-top tamarins with different sizes and compositions and study whether they remain stable after the birth of new infants. We also investigated the possible correlation between the time spent carrying infants and an increase in the grooming centrality. We found that group A (n = 13) had a stable grooming network that showed consistent stability after the birth, although group B (n = 8 and no adult helpers) changed its grooming network and showed a lower density after the birth. Infant carrying was not correlated with increased grooming centrality after the birth. These findings highlight the usefulness of social network analysis in the study of group structure in cooperatively breeding primates and suggest that the birth of offspring has a greater impact on the stability of groups without adult helpers.

Supplemental Material for Is Inferential Reasoning a Distinctly Human Cognitive Feature? Testing Reasoning in Cotton-Top Tamarins (Saguinus oedipus)

Supplemental Material for Is Inferential Reasoning a Distinctly Human Cognitive Feature? Testing Reasoning in Cotton-Top Tamarins (Saguinus oedipus)

Timing of the luteal-placental shift is delayed with additional fetuses in litter-bearing callitrichid monkeys, Saguinus oedipus and Callithrix jacchus

The luteal-placental shift is an important milestone of mammalian pregnancy signifying when endocrine control of pregnancy shifts from the corpus luteum of the ovary to the placenta. The corpus luteum is maintained by chorionic gonadotropin (CG). Upon sufficient placental maturation, CG production wanes, the corpus luteum involutes, and control is shifted to the placenta, one consequence of which is a midgestational rise in glucocorticoid production, especially cortisol and cortisone, by both mother and fetus. Glucocorticoids are involved in initiating parturition, prenatal programming of offspring phenotype, and maturing fetal organs. Limited evidence from human pregnancy suggests that the timing of this shift is delayed in twin pregnancies, but little is known about the timing of the luteal-placental shift in litter-bearing monkeys from the primate family Callitrichidae. Here we provide evidence from cotton-top tamarins (Saguinus oedipus) and common marmosets (Callithrix jacchus) of longer duration of elevated CG associated with multiple infant births compared to single births. Urinary profiles from cotton-top tamarins demonstrate that the decline of the extended elevation of CG precedes the onset of the midpregnancy sustained rise in glucocorticoids; this shift occurs later with an increase from one to two fetuses carried to term. In the common marmoset, the onset of the sustained rise of glucocorticoids in maternal urine is also delayed with an increase in infant number. Total urinary glucocorticoid levels during the last half of gestation increase monthly but do not differ by infant number. The significant delay in the luteal-placental shift suggests a longer period of placental maturation is needed to support a greater number of fetuses.

Consistent second-order motor planning by cotton-top tamarins (Saguinus oedipus): Evidence from a dowel task.

One of the hallmarks of complex motor planning in humans involves grasping objects in preparation for future actions, termed second-order motor planning. This ability has an extended developmental trajectory in humans and is also shared with nonhuman primates. Here, we presented seven cotton-top tamarins with a dowel task that has prompted variable grasping behaviors for some primate species. Tamarins could use either an efficient grasp to bring food stuck onto the end of a dowel to their mouth (radial grasp) or an inefficient grasp that required repositioning (ulnar grasp). The tamarins were very consistent in their use of radial grasps. These data support the morphological constraint theory suggesting that species with limited dexterity (inability to perform precision grasps) may demonstrate more consistent second-order motor planning due to the increased cost of inefficient grasping postures. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Proyecto Titi: Teaching children that cotton-top tamarins (Saguinus oedipus) are not appropriate pets.

Cotton-top tamarins (Saguinus oedipus) are a critically endangered species found only in Colombia. Their survival is threatened by extensive habitat destruction and the illegal pet trade. Because many people in Colombia have a low level of awareness of cotton-top tamarins and even less understanding of the impacts that the illegal pet trade has on the species and its long-term survival, Proyecto Tití has developed a series of programs for children in rural elementary schools that introduce children to cotton-top tamarins. This study examines Proyecto Titi's efforts to reduce the desire to have a cotton-top tamarin as a pet with outcomes focused specifically on (1) creating an emotional connection between people and cotton-top tamarins, (2) identifying the feelings and understanding the challenges that cotton-top tamarin face when they are kept as pets, and (3) empowering students to make positive choices to help cotton-top tamarins. Both TITI KIDS and TITIRITIANDO programs helped students to (1) increase their knowledge of cotton-top tamarins, (2) understand the damage that the pet trade has on individual animals and the long-term survival of cotton-top tamarins and (3) provide practical actions that they can engage in to protect cotton-top tamarins for the future. Our hope is that students from our programs become advocates for conservation in their communities and assist in the long-term conservation activities to protect cotton-top tamarins in Colombia.

Language preference in the domestic dog (Canis familiaris).

Studies have shown that both cotton-top tamarins as well as rats can discriminate between two languages based on rhythmic cues. This is similar to the capabilities of young infants, who also rely on rhythmic cues to differentiate between languages. However, the animals in these studies did not have long-term language exposure, so these studies did not specifically assess the role of language experience. In this study, we used companion dogs, who have prolonged exposure to human language in their home environment. These dogs came from homes where either English or Spanish was primarily spoken. The dogs were then presented with speech in English and in Spanish in a Headturn Preference Procedure paradigm to examine their language discrimination abilities as well as their language preferences. Dogs successfully discriminated between the two languages. In addition, dogs showed a novelty effect with their language preference such that Spanish-hearing dogs listened longer to English, and English-hearing dogs listened longer to Spanish. It is unclear what particular cue dogs are utilizing to discriminate between the two languages; future studies should explore dogs' utilization of phonological and rhythmic cues for language discrimination.

A modified version of the dimensional change card sort task tests cognitive flexibility in children (Homo sapiens) and cotton-top tamarins (Saguinus oedipus).

A modified Dimensional Change Card Sort (DCCS) task was used to test cognitive flexibility in adult cotton-top tamarins and children aged 19 months to 60 months. Subjects had to infer a rule from the experience of selecting between two cards to earn a reward, and the pairs of stimuli defined the rule (e.g., pick blue ones, not red ones, or pick trucks, not boats). Two different tests measured subjects' ability to shift to a reversal of the rule (intradimensional shift) and to shift to a new rule defined by a dimension previously irrelevant (interdimensional shift). Both adult tamarins and children aged 49-60 months were able to learn the initial rule and switch to a reversal and to a rule based on a different dimension. In contrast, the two younger groups of children, aged 19-36 months and aged 37-48 months, could switch when a reversal was imposed but took significantly longer to learn a new rule on a former irrelevant dimension. Experiment 2 presented a wider set of novel stimuli which shared some features with the original set to further explore the basis of rule learning. The result was that tamarins and 52- to 60-month-old children both chose novel stimuli that fit the rule and had no a priori associative strength, suggesting a rule application not solely based on associative strength. Importantly, novel items introduced some risk for choice, and children showed themselves to be risk-averse, whereas tamarins were risk-prone within a novel context. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Rules and metarules: Adult cotton-top tamarins (Saguinus oedipus) and 5-year-old children (Homo sapiens) can master both.

Developmental psychologists have noted a similar timeline of change for children's use of different perspectives about the same objects or events, as in the use of different labels for the same object, an aspect of language, and in understanding other's knowledge or beliefs, an aspect of social cognition as reviewed in the study by Neiworth et al. Comparative psychologists are interested to know what cognitive flexibility looks like in other species and how such variation relates to life history, ecology, and phylogeny. The general pattern of results to date indicates that monkeys can master both intra- and interdimensional shifts, but intradimensional shifts are learned far more quickly than interdimensional shifts (reviewed in the study by Neiworth et al, 2022). Neiworth et al. report that they have conducted exactly this kind of comparative study: They examined cognitive flexibility in adult cotton-top tamarins and human children in three age groups as they participated in a modified version of the Dimensional Change Card Sort (DCCS). Neiworth et al.'s study offers an example of careful consideration of one such possibility: that of using the experimenter's postural orientation to the cards as an inadvertent aid. Here the authors had the benefit of prior work showing that tamarins follow human-provided cues to make a spatially discriminated choice only if the experimenter's head, body, and eyes oriented to a particular location. Thus, in this study, the experimenter kept their head and body centered in the testing space between the two cards and looked at a point on the wall directly behind the midpoint of the testing tray. But the DCCS task, in abstract form, has potentially broader comparative value than to examine cognitive flexibility in primates alone. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

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.

Seasonality of reproduction in wild cotton‐top tamarins (Saguinus oedipus) in Colombia

Seasonal availability of resources can influence the timing and success of reproduction in primates. This study examines the annual pattern of conceptions, mid-term (13 weeks) and full-term (26 weeks) pregnancy losses, births, and infant survivorship of the Critically Endangered cotton-top tamarin (Saguinus oedipus) at Proyecto Tití's long-term field site in Santa Catalina, Colombia. Using 18 years of behavior, physical exam, and fecal steroid data (N = 51 females, 168 conceptions, 121 liters), fecal estrone conjugate (E1 C) and pregnanediol-3-glucuronide (PdG) or progesterone (P4) profiles were examined to investigate the relationships between female reproductive patterns and reproductive success with feeding and climatic data. Cotton-top tamarins demonstrated seasonal patterns of reproduction and pregnancy losses. We found positive correlations between peak conception and nectarivory, births and rainfall, and mid-lactation and frugivory. High body mass mothers reproducing during the peak season were more likely to have infants survive. Overall, these results suggest that tamarins use a "relaxed income-breeder" strategy. Cotton-top tamarins appear to maximize reproductive output at the time of ovulation, and can reduce their investment in the current reproductive effort at many stages. Changes in food availability due to habitat loss and climate change will require the Critically Endangered cotton-top tamarins to alter their reproductive strategies to survive.

Supplemental Material for Consistent Second-Order Motor Planning by Cotton-Top Tamarins (Saguinus oedipus): Evidence From a Dowel Task

Supplemental Material for Consistent Second-Order Motor Planning by Cotton-Top Tamarins (Saguinus oedipus): Evidence From a Dowel Task