Problem solving, inhibition and domain-specific experience: experiments on cottontop tamarins, Saguinus oedipus

We present the results of experiments on cottontop tamarins designed to explore the relationship between problem solving, inhibitory control and domain-specific experience. The colony was divided into two groups: tool-experienced (TE) and tool-inexperienced (TI). The TE group had previously participated in a series of tool-use experiments and revealed that, when selecting a tool, they used featurally relevant dimensions (e.g. shape, material, orientation) over featurally irrelevant dimensions (e.g. colour). The TI group, although experienced in other laboratory-based experiments, had never been tested on tool or other object manipulation problems. In Phase 1, involving three conditions, all subjects were tested on a series of means-end problems involving the use of a cloth to access a piece of food. Although the correct choice always involved picking the supporting cloth, we also built in an association between the correct cloth and its colour. Once the subjects reached criterion, we reversed the association between the cloth colour and the food reward in Phase 2. If the subjects solved the problems in Phase 1 by attending to cloth colour, then in Phase 2 they should have difficulty, especially given prior findings on tamarins demonstrating that reversal learning is difficult. If the subjects solved Phase 1 by attending to the functionality of the problem (i.e. the physical/causal relationship between the cloth and food), then reversing the colours in Phase 2 should have no effect on the subjects' performances. Finally, if the subjects attended to both colour and functionality, then reversing the colours should cause some decrement in performance, but less so than in the case where colour alone dominates. In Phase 2, although both groups showed a decrement in performance, indicating problems with reversal learning, TE subjects significantly outperformed TI subjects. Furthermore, the pattern of performance for TE subjects suggested that they had solved the initial problem by attending to a combination of colour and functionality or functionality alone, while TI subjects had attended to colour alone. We conclude that for tamarins with experience as tool users, colour represents a less salient feature, even when it is systematically associated with a food reward. For inexperienced tamarins, however, colour is salient and reversal learning is difficult. Together, these findings highlight the importance of exploring the relationship between inhibitory control and domain-specific problem solving. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Perception of harmonics in the combination long call of cottontop tamarins, Saguinus oedipus

A number of nonhuman primates produce vocalizations with time-varying harmonic structure. Relatively little is known about whether such spectral information plays a role in call type classification. We address this problem by utilizing acoustic analyses and playback experiments on cottontop tamarins‘ combi nation long call, a species-typical vocalization with a characteristic harmonic structure. Specifically, we used habituation-discrimination experiments to test whether particular frequency components, as well as the relationship between components, have an effect on the perception and classification of long calls. In Condition 1, we show that tamarins classify natural and synthetic exemplars of the long call as perceptually similar, thereby allowing us to use synthetics to manipulate components of this signal precisely. In subsequent conditions, we tested the perceptual salience and discriminability of long calls in which we deleted (1) the second harmonic, (2) the fundamental frequency, or (3) all frequencies above the fundamental; we also examined the effects of frequency mistuning by shifting the second harmonic by 1000 Hz. Following habituation to unmanipulated long calls, tamarins did not respond (transferred habituation) to long calls with either a missing fundamental frequency or the second harmonic, but responded (discriminated) to long calls with the upper harmonics eliminated or with the second harmonic mistuned. These studies reveal the importance of harmonic structure in tamarin perception, and highlight the advantages of using synthetic signals for understanding how particular acoustic features drive perceptual classification in nonhuman primates. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

A nonhuman primate's perception of object relations: experiments on cottontop tamarins, Saguinus oedipus

Objects in nature often have spatial and functional relationships with other objects. For example, fruit may be connected to tree branches, bushes sometimes function as landmarks for home, and stones are functionally associated with nuts when they are used to crack the nuts open. Although animals may use the spatial and functional relationships between specific objects, it is important for ethologists interested in cognitive mechanisms to ask whether animals understand the spatial relationship between objects in a more general and abstract way. In this experiment, we ask whether a small New World monkey, the cottontop tamarin, is capable of perceiving the abstract relational concept of ‘connectedness’. Using a traditional operant paradigm, subjects were required to press one button to images with connected objects, and another button to images with separated objects. In Phase 1 of the experiment, subjects received training with only one connected and one separated image. Following training, probe images were presented in which features such as colour, texture and shape were systematically manipulated to determine which features were more important in stimulus classification. Accuracies and reaction times of responses were recorded. On the basis of their performance, the tamarins appeared to recognize that changes in the colour or texture of two objects plays no functional role in determining whether such objects are connected or separated. In contrast, changes in the shape and distance between two objects does play an important functional role, and the tamarins appeared to be sensitive to such changes. In Phase 2, subjects received training with a larger set of images. After this training, classification accuracy remained significantly above chance with most probes, suggesting that the tamarins had acquired a more general connectedness concept. In Phase 3, novel images were presented. Classification accuracy was significantly above chance for many of the novel images. Overall, results suggest that tamarins perceive spatial relationships between stimuli to some extent and can classify images based in part on their spatial relationship. Other recent experiments have shown that cottontop tamarins respond to spatial relationships even better than in the current experiment when they have to act directly on the objects. The difference between these results suggests that tamarins perceive the spatial relationships between objects more readily in the context of an ecologically valid problem.     

Variations in care for cottontop tamarin, Saguinus oedipus, infants as a function of parental experience and group size

We examined the effects of parental experience and group size on infant care and development. Ten cottontop tamarin families were followed across three consecutive births of offspring to examine differences in survival, quality of care, developmental maturation and physical development for infants in two experimental conditions: (1) in large groups with previous parenting experience and (2) in small groups with little or no parenting experience. Although we found no differences in infant mortality, parents treated infants differently between conditions. However, when we examined the cumulative care provided by parents and sibling helpers together across experimental conditions, there were no differences in the rates of retrieval or rejection of infants. Overall levels of infant transport and food transfers were similar between conditions, with fathers and sibling helpers contributing the bulk of care. Fathers in small groups carried infants and transferred food with infants much more than helpers but, as group size increased, helpers augmented this role. Infant development varied with the experience of the family both between conditions and within a family. The results indicate that infants receive similar levels of care regardless of group size and parenting experience, although the individual contributions of family members change with both factors. Parental experience with previous infants had effects on early infant development, but only for the first sets of infants. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Scent-marking in the tamarin, Saguinus oedipus: Sex differences and ontogeny

Many mammalian species which exhibit scent-marking behaviour show a pronounced sexual dimorphism in marking behaviour and scent gland morphology. However, several species of marmosets and tamarins do not show dimorphism in these traits. We examined sex differences in scent-marking structures and behaviour in cotton-top tamarins (Saguinus o. oedipus; Primates: Callitrichidae). While body size and weight were virtually identical in adult males and females, there were pronounced sex differences in scent gland size and in rates of marking behaviour. Females possessed larger anogenital and suprapubic glands and showed 10-fold higher rates of anogenital marking and slightly higher rates of suprapubic marking than males. Observations on the development of anogenital marking revealed a lack of dimorphism during the first 2 years. Adult rates of anogenital marking in females were only observed in females housed separately from their natal family group. The onset of adult levels of marking behaviour corresponds with the adoption of the role of a breeding adult female, suggesting that anogenital marking plays a role in sexual communication.     

Sexual dimorphism in responses to unfamiliar intruders in the tamarin, Saguinus oedipus

Aspects of social structure in group-living species can be inferred by observing the responses of individuals to unfamiliar animals. This study examined the responses of mated pairs of cotton-top tamarins (Saguinus oedipus oedipus) to presentation of either unfamiliar conspecifics or members of a related tamarin species, the saddle-back tamarin (Saguinus fuscicollis fuscicollis). Male and female responses to intruders differed: resident males threatened, displayed piloerection, approached, and attacked intruders, especially males, while resident females showed increases in suprapubic scentmarking in the presence of intruders. Both males and females discriminated between the species of intruders, exhibiting more threats, scent-marking, piloerection, and approaches in the presence of conspecific intruders. There are pronounced sex differences in the signals and behaviour patterns that are elicited in an aggressive or territorial encounter with unfamiliar conspecifics in this monogamous primate.     

Social development during the first twenty weeks in the cotton-top tamarin (Saguinus o. oedipus)

Fourteen infant cotton-top tamarins from five captive family groups were studied during the first 20 weeks of life. We examined the roles of parents and of siblings of different ages as caregivers and as social companions for the infants, as well as the effects of group composition and group size on these roles. Parents and adult siblings played similar active roles in infant caregiving during the first few weeks after birth, with males showing a greater involvement than females. In groups without other offspring the two parents showed equal infant caregiving behaviour, whreas fathers carried more than mothers did in groups with offspring present. Although infants received more caregiving from males, they showed a preference for contact and proximity with their mothers. No sex differences were found in infant behaviour or in the direction of behaviour by caregivers toward infants. Twins showed greater amounts of both social and solitary play in weeks 15–20 than did singletons, and there was no effect of the number of older siblings on the amount of play shown by an infant.     

Multiple acoustic features underlie vocal signal recognition in tamarins: antiphonal calling experiments

We examine which acoustic features are relevant for recognition of the cotton-top tamarin (Saguinus oedipus) combination long-call. This vocalization, emitted by both males and females, functions in maintaining group cohesion, territory defense and mate attraction. Using the tamarins natural antiphonal vocal response to hearing a combination long-call as the primary measure of recognition, we presented subjects with synthetic exemplars of combination long-calls in which we manipulated across one of three acoustic dimensions: frequency, time and amplitude. Results indicated that although acoustic features in the frequency and time domains are important for combination long-call recognition, the changes in amplitude within and between syllables are not. Furthermore, while the fundamental frequency appears to be the used to encode information about the frequency contour, the temporal information is derived from the harmonics. Overall, these results suggest that tamarins use a specific suite of acoustic features for combination long-call recognition.Abbreviations CLC combination long-call - F0 fundamental frequency - JND just noticeable difference - JMD just meaningful difference - IPI inter-pulse interval     

Primary structure of carboxypeptidase T: Delineation of functionally relevant features in Zn-carboxypeptidase family

The primary structure of carobxypeptidase T—a Zn-dependent extracellular enzyme ofThermoactinomyces vulgaris—was determined from the clonedcpT gene nucleotide sequence and compared to Zn-carboxypeptidases from various organisms. The compilation and analysis of multiple alignment accompanied by consideration of available tertiary structure data have shown that in the overall spatial structure and active site arrangement CpT is similar to other enzymes constituting the Zn-carboxypeptidase family. Nine of 16 amino acid residues found to be strictly invariant are presumably located close to the active site. The preservation of His69, Glu72, Asn144, Arg145, His196, Tyr248, and Glu270 identified previously as essential catalytic site participants implicates basically the same catalytic mechanism in the Zn-carboxy-peptidase family. It is proposed that Pro205 and Asp256 should play an important role in proper S₁-pocket spatial arrangement. The comparative analysis of amino acid variations in S₁-pocket enabled us to reveal structural determinants of the Zn-carboxypeptidase primary specificity. The relatively reduced size of the pocket and negative charge of Asp253 are supposed to contribute correspondingly to A- and B-type substrate preferences of carboxypeptidase T endowed with dual primary specificity.     

Ontogeny of nesting habitat recognition and preference in neonatal herring gull chicks, Larus argentatus pontoppidan

The development of nesting habitat recognition and preferences in herring gull chicks was studied as a function of habitat and social stimuli. The test procedure consisted of relocating chicks 20 m from the nest and observing their movements. Results indicate that herring gull chicks exhibit a preference for the nest site area during the first week post-hatch, and this preference wanes after the first week until fledging. Chicks of all ages showed a preference for vegetation similar to that of the nest site area. Nest site preferences are ecotypically controlled. Vegetation characteristics, landmarks and the presence of other chicks were found to be among the cues used to recognize the nest site.     

Spontaneous tool use in captive, free-ranging golden lion tamarins (Leontopithecus rosalia rosalia)

Two types of tool use were observed in eight captive, free-ranging golden lion tamarins (Leontopithecus rosalia rosalia). All eight individuals used twigs and/or radio collar antennae to pry bark from trees and probe crevices, presumably for invertebrates. Three individuals used tools for grooming. In two animals, antennae were used as grooming tools while the third individual used a stick while grooming. The complexity of the free-ranging environment may have played a role in the expression of tool use behavior in these animals, as tool use has never been observed in captive tamarins living in traditional enclosures or wild tamarins. Social transmission may be one of the mechanisms responsible for the acquisition of tool use — six of the eight tool users resided in two social groups, and the only two individuals that used antennae as grooming tools were a bonded pair. These are the first published observations of tool use by golden lion tamarins or any callitrichid in a non-experimental setting and provide further data supporting the theory of a link between extractive foraging and tool use.     

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.     

Ontogeny of electroantennogram responses in the moth, Manduca sexta

The antennae of the moth, Manduca sexta, and the sensilla and sensory neurons they contain, develop during metamorphosis from pupa to adult. To determine when, during their development, antennae become capable of generating electrical responses to various stimuli, we recorded the electroantennogram (EAG), believed to be the summed extracellular record of receptor potentials, from developing and mature antennae. Antennae from male and female moths are similarly responsive to trans-2-hexenal, while only males respond to Manduca sex pheromone; these two odorants presumably stimulate separate receptors. Mechanical stimulation also elicits and EAG response. EAG responses to olfactory and mechanical stimuli are detectable several days before eclosion but not until the neurons are morphologically and biochemically quite mature. Responses increase in magnitude until the end of metamorphosis and then change little during the first 3 days after emergence of the adult. Responses to different stimuli do not develop synchronously.