Captive-born cotton-top tamarins (Saguinus oedipus) respond similarly to vocalizations of predators and sympatric nonpredators

What types of cues do callitrichid primates use to detect and respond to predators? Do they respond to predator‐specific cues or to more general cues? The evidence for these questions remains conflicting. We presented captive‐born and reared cotton‐top tamarins with no previous exposure to predators (or predator cues) with vocalizations from three potential predators of cotton‐top tamarin in the wild (white hawk, jaguar, and tayra) and with vocalizations from sympatric nonpredators (black‐faced antthrush and red howler monkey). Vocalizations from predators and from nonpredator mammals elicited equivalent arousal, fear, and vocal responses. Howler monkey roars produced the strongest responses. The results suggest that predator‐naïve cotton‐top tamarins do not recognize specific predator vocalizations, but may respond to vocal qualities (low‐frequency, noisy sounds) that indicate large body size, threat, or aggression. On the other hand, tamarins responded much more strongly to the higher frequency calls from the hawk than the antthrush, suggesting another mechanism must also be involved. The failure of captive‐reared tamarins to distinguish between vocalizations of predators and nonpredator mammals has important implications for reintroduction studies. Am. J. Primatol. 70:707–710, 2008. © 2008 Wiley‐Liss, Inc.     

The role of social context and individual experience in novel task acquisition in cottontop tamarins, Saguinus oedipus

In socially tolerant settings, na?ve individuals may have opportunities to interact jointly with knowledgeable demonstrators and novel tasks. This process is expected to facilitate social learning. Individual experience may also be important for reinforcing and honing socially acquired behaviours. We examined the role of joint interaction and individual experience in the acquisition of a novel foraging task in captive cottontop tamarins. The task involved learning how to locate and access two hidden food rewards from among 10 differently cued forage sites. Tamarins were tested in three different conditions: (1) individually, (2) while interacting with a na?ve mate, and (3) while interacting with a mate trained as a knowledgeable demonstrator. For tamarins tested with mates present, we interspersed social input test days with exposure to the task while alone. Tamarins were tested again 17 months after their last exposure to the task, to assess long-term memory. All tamarins tested with knowledgeable demonstrators solved the task. In contrast, tamarins tested alone or with na?ve mates had similarly high levels of neophobia and low levels of task acquisition. We conclude that joint interaction occurs in mated pairs of cottontop tamarins and facilitates the spread of novel behaviour. Interspersing test days with a knowledgeable demonstrator present and test days alone with the task helped tamarins to achieve the ultimate goal of the task: obtaining food rewards. Tamarins performed similarly when tested 17 months later, regardless of their initial learning environment. Tamarins had memory deficits for the location of hidden food rewards, but retained memory of the necessary motor actions and solved the task.     

Evidence for averaging of distance from landmarks in the domestic dog

Several studies in landmark use have shown that animals locate spatial positions by predominantly using perpendicular distance from extended surfaces over distance from individual landmarks. In the current study, I investigated whether the domestic dog encodes perpendicular distance from surfaces and whether they estimate distances from multiple cues. Dogs were first trained to locate a ball hidden at an equal and constant distance between an individual landmark and one wall (Experiment 1) or two walls (Experiment 2). On occasional unrewarded tests, the landmark was shifted laterally, perpendicularly or diagonally relative to one wall. Data revealed that the dogs largely determined where to search by averaging the distance from the walls of the room and the distance from the individual landmark. This study provides additional evidence that domestic dogs use metric properties of space to find a spatial location by use of landmarks. Although the present results are in accordance with the vector sum model, they are also consistent with current theories of spatial memory.     

Birth seasonality in cotton-top tamarins (saguinus oedipus) despite constant food supply and body weight

Goldizen et al. (1988) reported that wild saddle-back tamarins (Saguinus fuscicollis, Callitrichidae) show birth seasonality that is correlated with food supply and body weight. They suggested a sequence of ultimate causality in which shortage of food leads to reduced body weight which leads to timing of weaning and lactation when resources are more abundant. Cotton-top tamarins in captivity show birth seasonality despite constant food supply and body weight. Although natural availability of fruit and insects (which are key foods for tamarins) is related to rainfall, birth seasonality and body weight in captive cotton-top tamarins are unrelated to rainfall. The most likely proximate mechanism for seasonality of births in tamarins is photo-period, given existing data on populations living in natural and artificial lighting.     

Litter size and infant survivorship in wild groups of cotton‐top tamarins (Saguinus oedipus) in Colombia

Cotton‐top tamains (Saguinus oedipus) are a critically endangered primate found only in Colombia. Efforts to conserve this species are centered on developing effective management plans that integrate biological information regarding population dynamics and factors that influence their survival. This study documented infants born to wild cotton‐top tamarin females from 1994–2008 at two distinct field sites in northern Colombia. Our studies have shown that wild cotton‐top tamarins typically give birth to one litter each year and infant survival to 6 months of age was greater in the wild than has been reported in captive colonies. However, similar to reports from captive colonies, litter size of wild cotton‐top tamarins ranges from 1–3 infants, with twin litters most common. Here we report the first occurrence of triplet litters in nearly 20 years of observing wild cotton‐top tamarin groups. Over the first 3 months of life, wild‐born infants exhibited highest mortality during the first week of life, similar to reports from captive colonies. Infant survival in the wild also increases with successive litters as it does in captivity. However, inter‐birth interval, group size, and the number of adult males in the group did not appear to influence infant survival in the wild. The value of such long‐term data from field studies aids in the information that can be used to model future population trends and develop effective conservation plans for this critically endangered primate. Am. J. Primatol. 71:707–711, 2009. © 2009 Wiley‐Liss, Inc.     

Landmark Use by Cebus apella

We investigated the use of landmarks by capuchins to solve spatial search tasks. In Experiment 1 one subject learned to find a hidden reward in the middle of a 4-landmark configuration. During probe trials, with the landmark configuration expanded and no reward, the capuchin mainly searched near 2 of the 4 landmarks, thus showing it used the landmarks as beacons. In Experiment 2 two subjects learned to find a reward halfway between 2 landmarks, with the inter-landmark line variously oriented with respect to the room. During probe trials, with the landmark configuration expanded and no reward, the capuchins no longer searched in the middle of the landmark configuration. The capuchins searched between the landmarks, but at the training distance from each landmark separately. To do so, the capuchins may have memorized a certain distance to cover, beginning from a landmark, or exploited different types of perceptual information. Therefore, the capuchins use nearby landmarks to locate a goal, but not configurationally. We compare the results with those of previous studies with other animal species and discuss them in relation to issues of spatial cognition.     

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.     

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.     

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.     

Modeling monkeys: A comparison of computer-generated and naturally occurring foraging patterns in two species of neotropical primates

We present a series of computer-generated foraging models (random movement, olfactory navigation, and spatial memory) designed to examine the manner in which sensory cues and cognitive skills might be used by rainforest monkeys to locate patchily distributed feeding sites. These simulations are compared with data collected in the Amazon Basin of northeastern Peru on the foraging patterns of two species of neotropical primates, the moustached tamarin monkey (Saguinus mystax) and the saddle-back tamarin monkey (Saguinus fuscicollis). The results indicate that, although tamarins may rely on olfactory cues to locate nearby feeding sites, their foraging patterns are better explained by an ability to maintain a detailed spatial map of the location and distribution of hundreds of feeding trees in their home range. There is evidence that such informationis retained for a period of at least several weeks and is used to minimize the distance traveled between widely scattered feeding sites. The use of computer simulations provides a powerful research tool for generating predictive models regarding the role of memory and sensory cues in animal foraging patterns.     

Use of spatial, visual, and olfactory information during foraging in wild nocturnal and diurnal anthropoids: A field experiment comparing Aotus, Callicebus, and Saguinus

Early in their evolution, the ancestors of anthropoid primates radiated from a nocturnal to a diurnal niche. Foraging during the night differs from foraging during the day in terms of the availability of light and color cues, and in the movement of odor molecules through the canopy. In this study, we compared the ability of nocturnal and diurnal New World monkeys to use perceptual cues (i.e., the sight or smell of food) and spatial information (place predictability) in within-patch foraging decisions. An experimental field study was conducted on wild groups of night monkeys (Aotus nigriceps), tamarins (Saguinus imperator imperator and S. fuscicollis weddelli), and titi monkeys (Callicebus cupreus) at the Zoobotanical Park/UFAC, Rio Branco, Brazil. Our research design included the construction of feeding stations located in the home range of the study groups. Each feeding station consisted of eight visually identical feeding platforms located in a circular arrangement. In all test settings, two platforms at each feeding station contained a food reward (banana), and the remaining six platforms contained a sham reward (yellow plastic or inaccessible banana). In the night-monkey experiments, each feeding platform was illuminated by a 40-W red bulb to aid the researcher in observing their behavior. When the location of reward sites was predictable over time, individuals in all four species successfully relocated food rewards based solely on spatial information. Each species was also successful in using visual information to distinguish real from sham food rewards. However, only night monkeys and one group of emperor tamarins used olfactory information alone to locate food rewards. Overall, the species' performances did not clearly differentiate Aotus from diurnal New World primates in these experiments.     

Contributions to infant care in captive cotton-top tamarins (Saguinus oedipus): The influence of age,sex, and reproductive status

Marmosets and tamarins are characterized by a reproductive strategy that includes twinning, and a communal rearing system in which infant care is shared among all group members, both breeders and nonbreeding helpers (often older offspring). In order to test some predictions about the extent to which different age-sex classes should invest in infants, contributions to infant carrying and food-sharing by all family members were measured in captive groups of cotton-top tamarins (Saquinus oedipus) ranging in size from 2 to 12 independent individuals. Fourteen litters were observed from birth to 12 weeks. Carrying by mothers decreased steadily over the study period, while carrying by fathers and other offspring increased for 3–5 weeks, then declined. Infants spent more time carried by siblings than by either parent, but parents did more carrying than individual siblings and, also, shared more food with infants. Older siblings contributed more care than younger siblings did. Adult sons carried infants more than adult daughters did, but immature daughters carried more than immature sons did. However, adult daughters actively offered food to infants more than any other class of helper did. These results were interpreted in the light of hypotheses concerning the reproductive and dispersal strategies of callitrichid species.     

Temperature-metabolism relations in the cotton-top tamarin (Saguinus oedipus) model for ulcerative colitis

Examination of temperature-metabolism relations found no significant differences between thermoregulation of temperature housed laboratory cotton-top tamarins (Saguinus oedipus) and wild tamarins in Colombia, S.A. The results indicate that tamarins do not acclimate to a temperate environment and are metabolically stressed at T_a less than 32°C. This is consistent with an hypothesis of chronic metabolic stress as a factor in the etiology of cotton-top tamarin colitis, which is restricted to captive populations and not found in wild tamarins.     

Optimal foraging theory predicts effects of environmental enrichment in a group of adult golden lion tamarins

The success of environmental enrichment programs in effecting specific changes in the behavior of captive animals has not always been uniform. Separate studies demonstrated both an increase in food competition and a decrease in food competition among captive group-living primates upon introduction of foraging devices. The objectives of this study were to measure the effects of variation in resource distribution and availability on food competition in a group of captive adult golden lion tamarins (Leontopithecus rosalia). The resource variables chosen were suggested from optimal foraging theory. The energy invested to obtain an item influenced food transfer and aggressive behaviors while food abundance did not. All individuals obtained an equivalent number of items over the course of the experiment from the foraging device, even though some tamarins obtained most of their food rewards directly from the device while others received their food rewards primarily through food transfer from other group members. Because the monkeys appeared highly motivated to obtain food from the test apparatus and did not habituate to it, the foraging device used in this experiment could be used as regular environmental enrichment for golden lion tamarins. One way to circumvent potentially unacceptable rates of aggression, with this or any feeding protocol that increases foraging task complexity and search time, may be to provide more than one foraging device per group. Zoo Biol 17:231–244, 1998. © 1998 Wiley-Liss, Inc.     

Do female tamarins use visual cues to detect fruit rewards more successfully than do males?

Primates are unique among eutherian mammals for possessing trichromatic colour vision. It is generally proposed that trichromacy evolved to aid detection of ripe fruits against mature foliage. However, while trichromacy is routine in all Old World monkeys and apes (the catarrhines), a cone opsin polymorphism in New World monkeys (the platyrrhines) results in foraging groups with mixed capacities for chromatic distinction. Although 50-66% of female platyrrhines are trichromatic, all males are dichromatic. Here, we test the hypothesis that trichromatic platyrrhines use visual cues to detect fruit rewards more successfully than do males. Specifically, we ask whether female emperor tamarins, Saguinus imperator imperator, and saddleback tamarins, S. fuscicollis weddelli, are the first members of their foraging group to locate food patches; and, furthermore, whether they are more successful than males in using colour, shape and size cues to discriminate between sham and reward feeding sites. Our results show that females and males do not differ in their ability to locate or discriminate between feeding sites. We conclude that trichromatic vision in female tamarins does not confer an advantage for detecting yellow fruit rewards against mature foliage. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Colour discrimination learning in black-handed tamarin (<Emphasis Type="Italic">Saguinus midas niger</Emphasis>)

Colour is one cue that monkeys use for perceptual segregation of targets and to identify food resources. For fruit-eating primates such as Saguinus, an accurate colour perception would be advantageous to help find ripe fruits at distance. The colour vision abilities of black-handed tamarins (Saguinus midas niger) were assessed through a discrimination learning paradigm using Munsell colour chips as stimuli. Pairs of chips were chosen from an early experiment with protan and deutan humans. The monkeys (three males and one female) were tested with stimuli of the same hue, but different brightness values, in order to make sure that discriminations were based on colour rather than brightness cues. The results showed that the female, but not the males, presented an above-chance performance for stimuli resembling hue conditions under which tamarins forage (oranges vs greens). Colour vision in S. m. niger is discussed according to the advantages and disadvantages of dichromatism in daily search for food as well as to aspects regarding polymorphism in New World monkeys.     

Communication of food quality in captiveMacaca nemestrina and free-rangingAteles geoffroyi

While observational learning and social communication of feeding behavior have been demonstrated several times for edible foods, to date there has been no experimental evidence for learning to avoid distasteful or inedible foods by social cues in primates. A series of experiments on captive pigtail macaques (Macaca nemestrina) and free-ranging spider monkeys (Ateles geoffroyi) was performed to determine if members of these two species would avoid a food item that was rejected by a conspecific. The results indicated that, while individuals were capable of learning to avoid a distasteful food after personal experience, social cues were not sufficient to prevent other individuals from tasting the rejected foods or for discriminating between neutral and distasteful items. The results are discussed in terms of spacing patterns and visual access in the natural foraging situation.     

Contrafreeloading in grizzly bears: implications for captive foraging enrichment

Although traditional feeding regimens for captive animals were focused on meeting physiological needs to assure good health, more recently emphasis has also been placed on non‐nutritive aspects of feeding. The provision of foraging materials to diversify feeding behavior is a common practice in zoos but selective consumption of foraging enrichment items over more balanced “chow” diets could lead to nutrient imbalance. One alternative is to provide balanced diets in a contrafreeloading paradigm. Contrafreeloading occurs when animals choose resources that require effort to exploit when identical resources are freely available. To investigate contrafreeloading and its potential as a theoretical foundation for foraging enrichment, we conducted two experiments with captive grizzly bears (Ursus arctos horribilis). In Experiment 1, bears were presented with five foraging choices simultaneously: apples, apples in ice, salmon, salmon in ice, and plain ice under two levels of food restriction. Two measures of contrafreeloading were considered: weight of earned food consumed and time spent working for earned food. More free than earned food was eaten, with only two bears consuming food extracted from ice, but all bears spent more time manipulating ice containing salmon or apples than plain ice regardless of level of food restriction. In Experiment 2, food‐restricted bears were presented with three foraging choices simultaneously: apples, apples inside a box, and an empty box. Although they ate more free than earned food, five bears consumed food from boxes and all spent more time manipulating boxes containing apples than empty boxes. Our findings support the provision of contrafreeloading opportunities as a foraging enrichment strategy for captive wildlife. Zoo Biol 29:484–502, 2010. © 2009 Wiley‐Liss, Inc.     

Use of Social and Ecological Information in Tamarin Foraging Decisions

A major consequence of group living is that foragers may rely on social information in addition to ecological information to locate feeding sites. Although conspecifics can provide cues as to the spatial location of food patches, individual foraging decisions also must include some assessment of the likelihood of obtaining access to a resource other group members seek. This likelihood differs in the 2 models generally proposed to explain intragroup social foraging: the information-sharing model and the producer-scrounger model. We conducted an experimental field study on wild groups of emperor (Saguinus imperator) and saddleback (S. fuscicollis) tamarins to determine the foraging strategies adopted by individual group members and their relationship to social rank, food intake, and the ability to use ecological and social information in making intra-patch foraging decisions. Individual tamarins applied different behavioral strategies compatible with a finder-joiner paradigm to solve foraging problems. About half of the individuals in each study group initiated 74%–90% of all food searches and acted as finders. Most alpha individuals adopted a joiner strategy by monitoring the activities of others' to obtain a reward. The individual arriving first at a reward platform enjoyed a finder's advantage. Despite differences in search effort, both finders and joiners presented similar abilities in learning to associate ecological cues with the presence of food rewards at our experimental feeding stations. We conclude that within a group foraging context, tamarins integrate social and ecological information in decision-making.     

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.