Tamarins Research Articles

Variations in male parenting behavior and physiology in the common marmoset.

Infant survival and wellbeing is dependent upon good parenting skills. In some species of primates, fathers are necessary to ensure both positive developmental and social outcomes for their offspring. Common marmosets and the related cotton-top tamarin monkeys provide extensive paternal care of multiple offspring and are essential for infant survival. However, we have found significant variation in a father's motivation to respond to infant stimuli. Additionally, marmoset males who are experienced fathers are significantly more motivated to respond to infants and infant stimuli than adult males who have yet to be fathers. Expectant fathers appear to be preparing for their energetic role in infant care by responding with increases in multiple reproductive hormones and showing weight gain during their mate's pregnancy. Male marmosets have been shown to be hormonally responsive to scent signals. Males show increased testosterone shortly after smelling periovulatory scents and lower levels of testosterone following presentation of their own infant's scent. These two inverse testosterone responses combined indicate that paternal males have a flexible system of responding to socially relevant odor cues. Thus males can be ready to mate when their mate is fertile while continuing to be responsive to their infants when these two events occur simultaneously. A male's hormonal and physical responsiveness to parenting may be due to pair bonding between the male and his mate. Examining the variability between males in their behavioral, physical, and hormonal responses to their mate's pregnancy, and infant stimuli provides the means for determining the mechanisms of good parenting in fathers.

Cognitive preconditions for responses to fairness: An object retrieval test of inhibitory control in capuchin monkeys (Cebus apella).

The authors explore the evolution of one cognitive mechanism required for altruistic behavior: the capacity to inhibit prepotent responses. Specifically, the authors used an object retrieval task to investigate whether capuchins (Cebus apella) can inhibit a prepotent strategy of reaching directly for a food reward. Success in this task varies across species and across development, but is also known to depend critically on the maturity of dorsolateral prefrontal cortex, the cortical area implicated in rejecting small payoffs in an Ultimatum Game. Capuchins easily inhibit the tendency to reach directly for food in the object retrieval task, successfully employing an alternative reaching strategy even in the first session of performance. This contrasts with the performance of closely related tamarin monkeys, who performed less well despite extensive training. These results provide the first evidence that capuchins likely exhibit human-like inhibitory control in tasks previously linked to the function of the dorsolateral prefrontal cortex, such as the Ultimatum Game.

Hysteresis effects in a motor task with cotton-top tamarins (Sanguinus oedipus).

The way human adults grasp an object is influenced by their recent history of motor actions. Previously executed grasps are often more likely to reoccur on subsequent grasps. This type of hysteresis effect has been incorporated into cognitive models of motor planning, suggesting that when planning movements, individuals tend to reuse recently used plans rather than generating new plans from scratch. To the best of our knowledge, the phylogenetic roots of this phenomenon have not been investigated. Here, the authors asked whether 6 cotton-top tamarin monkeys (Saguinus oedipus) would demonstrate a hysteresis effect on a reaching task. The authors tested the monkeys by placing marshmallow pieces within grasping distance of a hole through which the monkeys could reach. On subsequent trials, the marshmallow position changed such that it progressed in an arc in either a clockwise or counterclockwise direction. The authors asked whether the transition point in right- versus left-handed reaches would differ depending on the direction of the progression. The data supported this hysteresis prediction. The outcome provides additional support for the notion that human motor planning strategies may have a lengthy evolutionary history.

Identification of postentry restrictions to Mason-Pfizer monkey virus infection in New World monkey cells.

TRIM5alpha has been shown to be a major postentry determinant of the host range for gammaretroviruses and lentiviruses and, more recently, spumaviruses. However, the restrictive potential of TRIM5alpha against other retroviruses has been largely unexplored. We sought to determine whether or not Mason-Pfizer monkey virus (M-PMV), a prototype betaretrovirus isolated from rhesus macaques, was sensitive to restriction by TRIM5alpha. Cell lines from both Old World and New World primate species were screened for their susceptibility to infection by vesicular stomatitis virus G protein pseudotyped M-PMV. All of the cell lines tested that were established from Old World primates were found to be susceptible to M-PMV infection. However, fibroblasts established from three New World monkey species specifically resisted infection by this virus. Exogenously expressing TRIM5alpha from either tamarin or squirrel monkeys in permissive cell lines resulted in a block to M-PMV infection. Restriction in the resistant cell line of spider monkey origin was determined to occur at a postentry stage. However, spider monkey TRIM5alpha expression in permissive cells failed to restrict M-PMV infection, and interference with endogenous TRIM5alpha in the spider monkey fibroblasts failed to relieve the block to infectivity. Our results demonstrate that TRIM5alpha specificity extends to betaretroviruses and suggest that New World monkeys have evolved additional mechanisms to restrict the infection of at least one primate betaretrovirus.

Do Humans Really Learn AnBn Artificial Grammars From Exemplars?

An important topic in the evolution of language is the kinds of grammars that can be computed by humans and other animals. Fitch and Hauser (F&H; 2004) approached this question by assessing the ability of different species to learn 2 grammars, (AB)(n) and A(n) B(n) . A(n) B(n) was taken to indicate a phrase structure grammar, eliciting a center-embedded pattern. (AB)(n) indicates a grammar whose strings entail only local relations between the categories of constituents. F&H's data suggest that humans, but not tamarin monkeys, learn an A(n) B(n) grammar, whereas both learn a simpler (AB)(n) grammar (Fitch & Hauser, 2004). In their experiments, the A constituents were syllables pronounced by a female voice, whereas the B constituents were syllables pronounced by a male voice. This study proposes that what characterizes the A(n) B(n) exemplars is the distributional regularities of the syllables pronounced by either a male or a female rather than the underlying, more abstract patterns. This article replicates F&H's data and reports new controls using either categories similar to those in F&H or less salient ones. This article shows that distributional regularities explain the data better than grammar learning. Indeed, when familiarized with A(n) B(n) exemplars, participants failed to discriminate A(3) B(2) and A(2) B(3) from A(n) B(n) items, missing the crucial feature that the number of As must equal the number of Bs. Therefore, contrary to F&H, this study concludes that no syntactic rules implementing embedded nonadjacent dependencies were learned in these experiments. The difference between human linguistic abilities and the putative precursors in monkeys deserves further exploration.

Grammatical pattern learning by human infants and cotton-top tamarin monkeys

There is a surprising degree of overlapping structure evident across the languages of the world. One factor leading to cross-linguistic similarities may be constraints on human learning abilities. Linguistic structures that are easier for infants to learn should predominate in human languages. If correct, then (a) human infants should more readily acquire structures that are consistent with the form of natural language, whereas (b) non-human primates’ patterns of learning should be less tightly linked to the structure of human languages. Prior experiments have not directly compared laboratory-based learning of grammatical structures by human infants and non-human primates, especially under comparable testing conditions and with similar materials. Five experiments with 12-month-old human infants and adult cotton-top tamarin monkeys addressed these predictions, employing comparable methods (familiarization–discrimination) and materials. Infants rapidly acquired complex grammatical structures by using statistically predictive patterns, failing to learn structures that lacked such patterns. In contrast, the tamarins only exploited predictive patterns when learning relatively simple grammatical structures. Infant learning abilities may serve both to facilitate natural language acquisition and to impose constraints on the structure of human languages.

Monkey See, Monkey Plan, Monkey Do

The way human adults grasp objects is typically influenced by their knowledge of what they intend to do with the objects. This influence is reflected in the end-state comfort effect: Actors adopt initially uncomfortable postures to accommodate later task demands. Although many experiments have demonstrated this effect, to the best of our knowledge its phylogenetic roots have not been investigated. In two experiments, we tested whether 9 cotton-top tamarin monkeys would show the end-state comfort effect. We did so by presenting the monkeys with a small cup containing a marshmallow. The cup was suspended in different orientations. The monkeys inhibited their natural grasping tendencies and adopted unusual grasping postures to accommodate subsequent task requirements, thus demonstrating the end-state comfort effect. This outcome provides evidence for more sophisticated motor planning than has previously been ascribed to this and related species.

Tree and forest characteristics influence sleeping site choice by golden lion tamarins

Lion tamarin monkeys are among a small number of primates that repeatedly use a few tree holes for the majority of their sleeping sites. To better understand why lion tamarins rely on tree holes as sleeping sites, we compared the physical characteristics of frequently used sleeping sites, infrequently used sleeping sites, and randomly selected forest locations at multiple spatial scales. From 1990 to 2004, we recorded 5,235 occurrences of sleeping site use by 10 groups of golden lion tamarins (Leontopithecus rosalia) in Poço das Antas Reserve, Rio de Janeiro State, Brazil. Of those, 63.6% were tree holes. Bamboo accounted for an additional 17.5% of observations. Frequently used tree holes were more likely to be found in living trees and their entrances were at lower canopy heights than infrequently used tree holes. We also found that frequently used sleeping sites, in comparison to random sites, were more likely to be found on hillsides, be close to other large trees, have a lower percent of canopy cover, and have larger diameter at breast height. Topography and small-scale variables were more accurate than were habitat-level classifications in predicting frequently used sleeping sites. There are ample tree holes available to these lion tamarins but few preferred sites to which they return repeatedly. The lion tamarins find these preferred sites wherever they occur including in mature forest and in relics of older forest embedded in a matrix of secondary forest.

Sleep quantitation in common marmoset, cotton top tamarin and squirrel monkey by non-invasive actigraphy

Sleep quantitation data on the Neotropical primate species, apart from the squirrel monkey, are still sparse. As such, we have quantitated sleep in the common marmosets ( Callithrix jacchus), cotton top tamarins ( Saguinus oedipus) and squirrel monkeys ( Saimiri sciureus) reared in one primate facility simultaneously, by non-invasive actigraphy. The range in total sleep time/24 h measured for male adult common marmosets, cotton top tamarins and squirrel monkeys were 713–793 min ( n = 4), 707–889 min ( n = 4) and 459–475 min ( n = 2) respectively. The range in sleep episode length /12 h dark phase for marmosets, tamarins and squirrel monkeys were 21–52 min ( n = 3), 10–28 min ( n = 4) and 9–15 min ( n = 2) respectively. Since vigilance is a critical evolutionary adaptive feature of predator avoidance among Callitrichid monkeys and squirrel monkeys, the shorter ranges in sleep episode length recorded, even under captivity, in this study could be interpreted as probable indicators of such vigilance behavior during the rest phase. We hypothesize that the vigilance behavior when it exists during a primate's active phase should also prevail when it is at rest (sleep). This hypothesis deserves additional testing in female Callitrichid monkeys.

Cotton-Top Tamarins' (Saguinus oedipus) Expectations About Occluded Objects: A Dissociation Between Looking and Reaching Tasks

Recent work with human infants and toddlers suggests a dissociation between performance on looking and reaching tasks. Specifically, infants appear to generate accurate representations of occluded objects and their actions when tested in expectancy violation looking tasks but often fail to use this information when reaching for occluded objects. We explore a similar dissociation in cotton-top tamarin monkeys (Saguinus oedipus). We presented adult tamarins with an event in which a piece of food rolled behind an occluder and into a solid barrier. In Experiment 1, subjects were required to retrieve the hidden food using the location of the solid barrier. Like human toddlers, adult tamarins failed to take into account solidity information when reaching for an invisibly displaced object. In Experiments 2 and 3, we presented subjects with expectancy violation looking versions of the same solidity problem using an identical apparatus and setup. We presented subjects with an event in which a piece of food appeared to roll unexpectedly through a solid barrier or stopped at the appropriate spot. Although tamarins failed to locate the food in Experiment 1, the same subjects successfully detected violations of solidity in these 2 looking studies. This performance dissociation is discussed in light of similar dissociations in human toddlers and other primate species.

Decision Making: The Virtue of Patience in Primates

Marmoset monkeys devalue rewards requiring travel to acquire, but tamarin monkeys do not, despite the greater patience of marmosets when rewards are delayed in time. Such preference reversals, not predicted by standard economic theory, may reflect behavioral mechanisms adaptively specialized for different spatial and temporal patterns of foraging.

Acute GB virus B infection of marmosets is accompanied by mutations in the NS5A protein

GBV-B, a member of the Flaviviridae family of viruses, is the virus most closely related to HCV, and GBV-B infection in tamarin monkeys might represent a valuable surrogate animal model of HCV infection. In the current study, GBV-B was successfully transmitted to two marmosets ( Callithrix jaccus). The infection resulted in viremia of 14- and 17-week duration, respectively, and was accompanied by elevation of isocitrate dehydrogenase activity. These data confirm that marmosets might represent an attractive model for GBV-B infection. The sequence of GBV-B NS5A, which was previously reported to have one of the highest mutation rates during infection in tamarins, was determined for viruses recovered from the inoculum and from marmoset blood samples obtained at weeks 1, 8, and 14 post inoculation in one marmoset and at weeks 2, 8, and 17 post inoculation in the other marmoset. In both animals, we detected four substitutions (R1945K, K2052G, F2196L, and G2268E), in the virus recovered immediately before viral clearance. Interestingly, two of these mutations (F2196L and G2268E) were described recently for viruses recovered from persistently infected tamarins. Appearance of these mutations presumably reflects a mechanism of immune escape rather than adaptation of the virus to a new host.

Dinucleotide microsatellite primers designed for a critically endangered primate, the black lion tamarin (Leontopithecus chrysopygus)

AbstractBlack lion tamarin (BLT) monkeys (Leontopithecus chrysopygus) have suffered a severe reduction in their natural range and are consequently critically endangered. Because allozyme data showed very low levels of variation, it was not clear if these monkeys had much genetic diversity. We designed microsatellite primers for BLTs, and from them we identified nine polymorphic loci, seven of which were tested on golden lion tamarins (GLTs) (Leontopithecus rosalia). All of the seven polymorphic loci and two other monomorphic BLT loci were polymorphic in GLTs. The microsatellite markers identified here are directly applicable to ongoing lion tamarin population and conservation genetics studies.

Modeling reciprocation and cooperation in primates: evidence for a punishing strategy

Experiments in which animals strategically interact with one another or search over some controlled domain are becoming common. While these experiments often promise to illuminate sophisticated animal behavior, the analyses brought to bear on these data are often quite coarse. For example, many papers simply tally the number of observations consistent with a behavioral theory. This analysis is simple, but ignores a potentially rich source of information by failing to take into account patterns and systematic variation among observations inconsistent with the theory. Using a new data set generated by cotton-top tamarin monkeys playing a repeated food-exchange game, we apply a maximum-likelihood estimation technique (more commonly used to study human economic behavior) which utilizes much more of the information in these data, and which uncovers unexpectedly sophisticated cooperative behavior from our subjects. Tamarin cooperation remains stable as long as both actors consistently cooperate, but requires at least two consecutive unexpected acts of cooperation to restart cooperation after it has collapsed, a strategy that resembles two-tits for a tat. We conclude by enumerating the benefits of a maximum-likelihood approach in experimental settings such as ours, and suggest other areas in which these techniques may be fruitful.

Book Review: Marc Hauser. 2000. Wild Minds: What Animals Really Think. Henry Holt and Company, New York, 315 pp. $15.00 (Paperback)

What do you conclude when a spider monkey throws her arms around your neck and coos? This is the first question Marc Hauser asks as he unfolds his extensive exploration of animal minds. Written for a wide audience including the nonexpert, Wild Minds carefully dissects animal behavior to understand exactly what we can and cannot conclude about the way animal minds function. In the prologue, Hauser is quick to say that he thinks questions like ‘Do animals think?’ or ‘Are some animals more intelligent than others?’ are not helpful. Instead, he asks more focused questions to illuminate precisely what an experiment has shown. When a tamarin monkey uses a cane to pull inaccessible food forward, does she understand the cane as a tool, or would she pull any similarly colored object towards her? When bees ignore the dance of a forager who seems to be indicating that food is in the middle of a lake, do they actually have a mental map of the area? Our culture is not known for its consistency in dealing with animals. Disney dresses them in human clothes and makes them talk; but we also raise them, often carelessly, for food. Our pets are smart, but they are certainly not in the same moral category as our children. This makes it particularly tough to objectively consider the idea of animal intelligence. Much of our conception of animal minds comes from anecdotes like the story of Binty, the gorilla at the Chicago zoo, who ‘saved’ the little boy after he fell into the enclosure or like the reports of dogs finding their owners after a cross-country trek. Hauser is critical of anecdotal evidence particularly when it includes the language of intention. To say that an animal ‘wants’ this or that is overlaying our mental framework where it might not belong. Notions of compassion or empathy are traps when interpreting animal behavior. For Hauser, repeatability is the key measure of soundness, but he is not ruthless about discarding data. Many of our observations of the animal world, particularly in natural surroundings, have to be of the one-of-a-kind variety. Hauser recognizes this and uses these observations to ask additional questions that perhaps can be resolved in more controlled settings. Marc Hauser is a professor of psychology and neuroscience at Harvard University. In Wild Minds, he displays a solid grasp of the animal behavior literature

Comparative morphological studies on the stereo structure of the lingual papillae of selected primates using scanning electron microscopy

A scanning electron microscope was used to observe the lingual papillae and their connective tissue cores (CTCs) in five primates (tupai, tamarin, crab-eating monkey, mandrill, and human). There were some slender protrusions rising from the top of the filiform papilla in all five types of primate. After removing the epithelium the filiform CTC from the tupai, tamarin and crab-eating monkey displayed a U-shaped arrangement of rod-shaped protrusions. The filiform CTC from the crab-eating monkey also had a columnar base. The human filiform CTC consisted of a primary columnar base, numerous short rod-shaped secondary protrusions from its upper periphery, and a few central protrusions. The filiform CTC from the Mandrill was fundamentally similar to that of the human, however, its base was shorter. The fungiform CTC from the tupai was column shaped, with several depressions for taste buds on the top. There were three vallate papillae in the tupai, tamarin, and mandrill, approximately four in the monkey, and between five and twelve in the human. Moderately developed foliate papillae were found in the tamarin, monkey, mandrill and human. The tupai, however, possessed a finger-like lateral organ instead. The lingual root area of the tupai, tamarin, crab-eating monkey and mandrill was relatively small with a smooth surface. Only the human had a tonsil-structure, which was located on the surface of its larger lingual root.

Learning at a distance II. Statistical learning of non-adjacent dependencies in a non-human primate

In earlier work we have shown that adults, infants, and cotton-top tamarin monkeys are capable of computing the probability with which syllables occur in particular orders in rapidly presented streams of human speech, and of using these probabilities to group adjacent syllables into word-like units. We have also investigated adults’ learning of regularities among elements that are not adjacent, and have found strong selectivities in their ability to learn various kinds of non-adjacent regularities. In the present paper we investigate the learning of these same non-adjacent regularities in tamarin monkeys, using the same materials and familiarization methods. Three types of languages were constructed. In one, words were formed by statistical regularities between non-adjacent syllables. Words contained predictable relations between syllables 1 and 3; syllable 2 varied. In a second type of language, words were formed by statistical regularities between non-adjacent segments. Words contained predictable relations between consonants; the vowels varied. In a third type of language, also formed by regularities between non-adjacent segments, words contained predictable relations between vowels; the consonants varied. Tamarin monkeys were exposed to these languages in the same fashion as adults (21 min of exposure to a continuous speech stream) and were then tested in a playback paradigm measuring spontaneous looking (no reinforcement). Adult subjects learned the second and third types of language easily, but failed to learn the first. However, tamarin monkeys showed a different pattern, learning the first and third type of languages but not the second. These differences held up over multiple replications, using different sounds instantiating each of the patterns. These results suggest differences among learners in the elementary units perceived in speech (syllables, consonants, and vowels) and/or the distance over which such units can be related, and therefore differences among learners in the types of patterned regularities they can acquire. Such studies with tamarins open interesting questions about the perceptual and computational capacities of human learners that may be essential for language acquisition, and how they may differ from those of non-human primates.

Give unto others: genetically unrelated cotton-top tamarin monkeys preferentially give food to those who altruistically give food back

Altruistic food giving among genetically unrelated individuals is rare in nature. The few examples that exist suggest that when animals give food to unrelated others, they may do so on the basis of mutualistic or reciprocally altruistic relationships. We present the results of four experiments designed to tease apart the factors mediating food giving among genetically unrelated cotton-top tamarins (Saguinus oedipus), a cooperatively breeding New World primate. In experiment 1 we show that individuals give significantly more food to a trained conspecific who unilaterally gives food than to a conspecific who unilaterally never gives food. The apparent contingency of the tamarins' food-giving behaviour motivated the design of experiments 2-4. Results from all three experiments show that altruistic food giving is mediated by prior acts of altruistic food giving by a conspecific. Specifically, tamarins do not give food to unrelated others when the food received in the past represents the by-product of another's selfish actions (experiments 2 and 3) or when a human experimenter gives them food (experiment 4) as did the unilateral altruist in experiment 1. By contrast, if one tamarin gives another food without obtaining any immediate benefit, then the recipient is more likely to give food in return. Overall, results show that tamarins altruistically give food to genetically unrelated conspecifics, discriminate between altruistic and selfish actions, and give more food to those who give food back. Tamarins therefore have the psychological capacity for reciprocally mediated altruism.

The use of prosodic cues in language discrimination tasks by rats.

Recent research with cotton-top tamarin monkeys has revealed language discrimination abilities similar to those found in human infants, demonstrating that these perceptual abilities are not unique to humans but are also present in non-human primates. Specifically, tamarins could discriminate forward but not backward sentences of Dutch from Japanese, using both natural and synthesized utterances. The present study was designed as a conceptual replication of the work on tamarins. Results show that rats trained in a discrimination learning task readily discriminate forward, but not backward sentences of Dutch from Japanese; the results are particularly robust for synthetic utterances, a pattern that shows greater parallels with newborns than with tamarins. Our results extend the claims made in the research with tamarins that the capacity to discriminate languages from different rhythmic classes depends on general perceptual abilities that evolved at least as far back as the rodents.

Hepatitis C Virus (HCV)

1.1 Characteristics of HCV HCV is the sole virus species of the genus Hepacivirus which, together with the genera Flavivirus and Pestivirus, constitutes the Flaviviridae family of viruses [1, 2]. The genera Hepacivirus and Pestivirus are structurally and biologically more closely related to one another than to the genus Flavivirus. Unlike Flavivirus, neither requires arthropods as vectors, and both may cause persistent infections in mammals. HCV is similar to the GB virus type B (GBV-B) that causes hepatitis in tamarin monkeys. Less closely related to HCV are GBV-A in various New World monkeys and GBV-C in humans [2], which to date has no known pathogenicity. The virus particles of Flaviviridae are surrounded by a lipid envelope in which at least two glycosylated surface proteins are anchored: E1 and E2 in the case of the genera Hepacivirus and Pestivirus, M and E in the case of the genus Flavivirus. (Pestiviruses additionally contain an E^rns). The viral envelope encloses a core particle formed from core protein and the single- stranded genome RNA with approximately 9,600 bases (in the case of HCV). Since only modest amounts of HCV can be isolated from plasma, the structure of the virus particles has not yet been exhaustively investigated. The hypothetical model in figure 1 has been inferred from knowledge about other Flaviviridae. ...