A comparison between common marmosets (Callithrix jacchus) and human infants sheds light on traits proposed to be at the root of human octave equivalence.

Two notes separated by a doubling in frequency sound similar to humans. This "octave equivalence" is critical to perception and production of music and speech and occurs early in human development. Because it also occurs cross-culturally, a biological basis of octave equivalence has been hypothesized. Members of our team previousy suggested four human traits are at the root of this phenomenon: (1) vocal learning, (2) clear octave information in vocal harmonics, (3) differing vocal ranges, and (4) vocalizing together. Using cross-species studies, we can test how relevant these respective traits are, while controlling for enculturation effects and addressing questions of phylogeny. Common marmosets possess forms of three of the four traits, lacking differing vocal ranges. We tested 11 common marmosets by adapting an established head-turning paradigm, creating a parallel test to an important infant study. Unlike human infants, marmosets responded similarly to tones shifted by an octave or other intervals. Because previous studies with the same head-turning paradigm produced differential results to discernable acoustic stimuli in common marmosets, our results suggest that marmosets do not perceive octave equivalence. Our work suggests differing vocal ranges between adults and children and men and women and the way they are used in singing together may be critical to the development of octave equivalence. RESEARCH HIGHLIGHTS: A direct comparison of octave equivalence tests with common marmosets and human infants Marmosets show no octave equivalence Results emphasize the importance of differing vocal ranges between adults and infants.

Temporal consistency and ecological validity of personality structure in common marmosets (Callithrix jacchus): A unifying field and laboratory approach.

Personality in animals has been extensively researched in recent decades. Temporal consistency of behaviors is almost always part of the personality definition and is usually explored in several different testing sessions or observation periods. However, it is still unclear whether the obtained personality constructs are stable across several years, which might be especially important for long-living animals, such as primates. Further, little is known on whether the personality structures obtained in the laboratory reflect the structures obtained under ecologically relevant conditions in the wild. Therefore, we conducted a battery of personality tests on common marmosets (Callithrix jacchus) (N = 27), compared it with a test battery conducted 4 years beforehand on a subset of animals in captivity (N = 13) and ran an adapted version under field conditions at Baracuhy Biological Field Station, Brazil (N = 18). Under captive conditions, we found a remarkably similar personality structure across 4 testing years. Further, we found high long-term temporal consistency in the first two personality components, Boldness and Exploration; however, monkeys that changed their social (i.e., breeding) status between the two testing periods showed a significant increase in Boldness scores. Under field conditions, we found a somewhat similar personality structure as compared to the laboratory, which to some extent corroborates ecological validity of our personality test design. Nevertheless, whether the structure in the wild is suppressed or expanded in comparison to captivity, and in which way the social setting influences personality structure, should be further explored. Taken together, our results contribute to the discussion about the reliability and ecological validity of personality structures in nonhuman primates.

Common marmosets are sensitive to simple dependencies at variable distances in an artificial grammar.

Recognizing that two elements within a sequence of variable length depend on each other is a key ability in understanding the structure of language and music. Perception of such interdependencies has previously been documented in chimpanzees in the visual domain and in human infants and common squirrel monkeys with auditory playback experiments, but it remains unclear whether it typifies primates in general. Here, we investigated the ability of common marmosets (Callithrix jacchus) to recognize and respond to such dependencies. We tested subjects in a familiarization-discrimination playback experiment using stimuli composed of pure tones that either conformed or did not conform to a grammatical rule. After familiarization to sequences with dependencies, marmosets spontaneously discriminated between sequences containing and lacking dependencies ('consistent' and 'inconsistent', respectively), independent of stimulus length. Marmosets looked more often to the sound source when hearing sequences consistent with the familiarization stimuli, as previously found in human infants. Crucially, looks were coded automatically by computer software, avoiding human bias. Our results support the hypothesis that the ability to perceive dependencies at variable distances was already present in the common ancestor of all anthropoid primates (Simiiformes).

A technological framework for running and analyzing animal head turning experiments.

Head turning experiments are widely used to test the cognition of both human infants and non-human animal species. Monitoring head turns allows researchers to non-invasively assess attention to acoustic or visual stimuli. In the majority of head turning experiments, the head direction analyses have been accomplished manually, which is extremely labor intensive and can be affected by subjectivity or other human errors and limitations. In the current study, we introduce an open-source computer program for measuring head directions of freely moving animals including common marmoset monkeys (Callithrix jacchus), American alligators (Alligator mississippiensis), and Mongolian gerbils (Meriones unguiculatus) to reduce human effort and time in video coding. We also illustrate an exemplary framework for an animal head turning experiment with common marmoset monkeys. This framework incorporates computer-aided processes of data acquisition, preprocessing, and analysis using the aforementioned software and additional open-source software and hardware.

Consistent inter-individual differences in common marmosets (Callithrix jacchus) in Boldness-Shyness, Stress-Activity, and Exploration-Avoidance.

The study of animal personality, defined as consistent inter-individual differences in correlated behavioral traits stable throughout time and/or contexts, has recently become one of the fastest growing areas in animal biology, with study species ranging from insects to non-human primates. The latter have, however, only occasionally been tested with standardized experiments. Instead their personality has usually been assessed using questionnaires. Therefore, this study aimed to test 21 common marmosets (Callithrix jacchus) living in three family groups, in five different experiments, and their corresponding controls. We found that behavioral differences between our animals were not only consistent over time, but also across different contexts. Moreover, the consistent behaviors formed a construct of four major non-social personality components: Boldness-Shyness in Foraging, Boldness-Shyness in Predation, Stress-Activity, and Exploration-Avoidance. We found no sex or age differences in these components, but our results did reveal differences in Exploration-Avoidance between the three family groups. As social environment can have a large influence on behavior of individuals, our results may suggest group-level similarity in personality (i.e., "group personality") in common marmosets, a species living in highly cohesive social groups. Am. J. Primatol. 78:961-973, 2016. © 2016 Wiley Periodicals, Inc.

Personality and social environment predict cognitive performance in common marmosets (Callithrix jacchus).

Consistent inter-individual variation in cognition has been increasingly explored in recent years in terms of its patterns, causes and consequences. One of its possible causes are consistent inter-individual differences in behaviour, also referred to as animal personalities, which are shaped by both the physical and the social environment. The latter is particularly relevant for group-living species like common marmosets (Callithrix jacchus), apt learners that display substantial variation in both their personality and cognitive performance, yet no study to date has interlinked these with marmosets' social environment. Here we investigated (i) consistency of learning speed, and (ii) whether the PCA-derived personality traits Exploration-Avoidance and Boldness-Shyness as well as the social environment (i.e., family group membership) are linked with marmosets' speed of learning. We tested 22 individuals in series of personality and learning-focused cognitive tests, including simple motor tasks and discrimination learning tasks. We found that these marmosets showed significant inter-individual consistency in learning across the different tasks, and that females learned faster than males. Further, bolder individuals, and particularly those belonging to certain family groups, learned faster. These findings indicate that both personality and social environment affect learning speed in marmosets and could be important factors driving individual variation in cognition.

Age, but not hand preference, is related to personality traits in common marmosets (Callithrix jacchus).

The proximate mechanisms underlying animal personalities, i.e. consistent inter-individual differences in behaviour, are a matter of discussion. Brain lateralization, expressed as the preferred use of the contralateral limb, has been suggested as one of these mechanisms. In this study, we measured a proxy of brain lateralization in captive common marmosets (N = 28) by testing hand preference in a simple food-reaching task and evaluated personality by coding a wide range of behaviours observed in daily situations. We explored the links between personality and both direction and strength of hand preference, as well as age and sex, using linear models. Principal component analysis revealed that the stable behavioural variables were organized in three personality dimensions: Agreeableness, Extraversion and Neuroticism. Regarding hand preference, 14 individuals were left-handed, seven were right-handed and seven were ambilateral. Contrary to our predictions, we did not find any relationship between personality scores and hand preference or sex. Instead, age was a significant predictor of personality scores, with older individuals being more agreeable and less extraverted. The link between brain lateralization and personality seems to be equivocal and dependent on personality and brain lateralization assessment methods. Further examinations of other proximate mechanisms, such as physiology or (epi)genetics, may elucidate what drives personality variation in common marmosets.

"How not to judge a deer by its cover": A personality assessment study on captive adult red deer males (Cervus elaphus).

Personality is not a uniquely human characteristic and it has been documented in a wide range of organisms, from mammals to birds, reptiles, fish, and invertebrates. However, personality is still poorly understood in Cervids. Therefore, our study aimed to fill this gap by i) investigating personality and ii) exploring its links to dominance hierarchy, assessed by behavioral observations in 11 captive and tame male red deer (Cervus elaphus). Using questionnaires to assess personality, three trained volunteers rated these animals in 15 behaviorally composed adjectives with detailed descriptions, based on their overall impression at the end of the observation period. Behavioral data from animals were collected across three different situations, namely "feeding" (i.e., high competition for a scarce resource), "normal" (i.e., no external stimuli) in a group setting, and "handling" (i.e., stressful situation due to human manipulation) in an individual setting. We estimated dominance hierarchies between the individuals based on situations of average and high competition (i.e., "normal" and "feeding") via the Clutton-Brock Index (CBI). Using Fleiss' Kappa for inter-rater reliability, only five of our 15 behavioral adjectives showed acceptable reliability. Using principal component analysis, four of these adjectives formed one personality component labelled "Confidence/Aggressiveness". We found that although "Confidence/Aggressiveness" did not correlate with CBI, ratings of two adjectives loading onto this component, namely "Confident" and "Submissive", significantly correlated with the CBI, indicating that the questionnaire ratings reflect real behavioral variation in red deer males. Our study provides the first assessment of personality in male red deer and adds to the growing literature on Cervid personality, offering the basis for future personality research in ungulates.

Comparative assessment of behaviorally derived personality structures in golden-handed tamarins (Saguinus midas), cotton-top tamarins (Saguinus oedipus), and common marmosets (Callithrix jacchus).

One way to address questions about the origins and adaptive significance of personality dimensions is by comparing the personality structures of closely related species that differ in their socioecological circumstances. For the present study, we compared the personalities of captive golden-handed tamarins (Saguinus midas; N = 28), cotton-top tamarins (Saguinus oedipus; N = 20), and common marmosets (Callithrix jacchus; N = 17). All 3 species are New World monkeys of the family Callitrichidae. They thus share reproductive and behavioral characteristics but differ some in terms of their diet, habitat, and social organization. We expected that personality structures of closely related tamarin species would overlap more, both in terms of number of dimensions and their content, than either would overlap with the personality structure of common marmosets. We assessed personality using behavioral observations and compared the personality structures by means of cross-species correlations and fuzzy set analyses. Principal component analyses identified components that we labeled Agreeableness, Assertiveness, and Extraversion in golden-handed tamarins and common marmosets and components labeled Confidence and Extraversion in cotton-top tamarins. The greater personality similarities of the two phylogenetically more distant species suggest that differences in social organization, and in both habitat diversity and complexity, contributed to the evolution of personality. However, we also found that behaviors clustered in similar ways in the two tamarin species, suggesting that phylogenetic relatedness and genus-specific socioecological characteristics, such as the degree of reproductive competition, shaped personality structure in this primate family. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Personality method validation in common marmosets (Callithrix jacchus): Getting the best of both worlds.

Animal personality, consistent interindividual differences in behavior through time, has been intensively studied across animal taxa and particularly in nonhuman primates. Two different methods have been used to study personality: questionnaires filled out by trusted raters, following the research tradition in human personality psychology, and behavioral observations or testing, based on the behavioral ecology research tradition. Systematic research of cross-method validity has, however, brought equivocal results. Here we report a systematic method comparison with strict validation criteria in common marmosets (Callithrix jacchus). We compared questionnaire data, observational behavioral data, and experimentally assessed behavioral data independently collected in two different research laboratories and across two years. Notably, we constructed a priori predictions on the degree and direction of correlations between the questionnaire-derived constructs and behaviorally derived constructs/variables. Convergent validity of the constructs/variables was present but was not found in both laboratories for any of the constructs. Discriminant validity was found to some degree for all constructs in both laboratories, with important exceptions. It seems that marmoset personality structure obtained with descriptor ratings does not consistently capture the predicted behavioral variables. Our finding that these two methods do not quite reach common ground thus urges caution in the choice of the suitable methods to study personality in nonhuman primates. We discuss the directions to which animal personality research should go so that it can get the "best of both worlds." (PsycINFO Database Record (c) 2020 APA, all rights reserved).

An Introduction to the Callithrix Genus and Overview of Recent Advances in Marmoset Research.

We provide here a current overview of marmoset (Callithrix) evolution, hybridization, species biology, basic/biomedical research, and conservation initiatives. Composed of 2 subgroups, the aurita group (C aurita and C flaviceps) and the jacchus group (C geoffroyi, C jacchus, C kuhlii, and C penicillata), this relatively young primate radiation is endemic to the Brazilian Cerrado, Caatinga, and Atlantic Forest biomes. Significant impacts on Callithrix within these biomes resulting from anthropogenic activity include (1) population declines, particularly for the aurita group; (2) widespread geographic displacement, biological invasions, and range expansions of C jacchus and C penicillata; (3) anthropogenic hybridization; and (4) epizootic Yellow Fever and Zika viral outbreaks. A number of Brazilian legal and conservation initiatives are now in place to protect the threatened aurita group and increase research about them. Due to their small size and rapid life history, marmosets are prized biomedical models. As a result, there are increasingly sophisticated genomic Callithrix resources available and burgeoning marmoset functional, immuno-, and epigenomic research. In both the laboratory and the wild, marmosets have given us insight into cognition, social group dynamics, human disease, and pregnancy. Callithrix jacchus and C penicillata are emerging neotropical primate models for arbovirus disease, including Dengue and Zika. Wild marmoset populations are helping us understand sylvatic transmission and human spillover of Zika and Yellow Fever viruses. All of these factors are positioning marmosets as preeminent models to facilitate understanding of facets of evolution, hybridization, conservation, human disease, and emerging infectious diseases.

Artificial visual stimuli for animal experiments: An experimental evaluation in a prey capture context with common marmosets (Callithrix jacchus).

Experimenters often use images of real objects to simulate interactions between animal subjects or visual stimuli on a touchscreen to test animal cognition. However, the degree to which nonhuman animals recognize 2-D images as representing the corresponding real objects remains debated. The common marmoset monkey (Callithrix jacchus) has been described as a species that spontaneously shows natural behaviors to 2-D images, for example, grasping behaviors to insects and fear responses to snakes. In this study, we tested 10 monkeys with their favorite food item (crickets), 2-D images (a photo and videos of a cricket), and a 3-D plastic model to reevaluate marmoset's spontaneous responses to 2-D images and to explore which artificial visual stimuli can motivate spontaneous interactions. The monkeys showed grasping behavior to the real cricket and the 3-D plastic model, but to none of the 2-D images. Our experiment suggests that depth information is the most important factor eliciting predatory behavior from the marmosets, and, therefore, a stimulus produced by a 3-D printer could be a good alternative when a spontaneous interaction or a convincing stimulus is required. Furthermore, this work serves as a cautionary tale for those using 2-D image presentations with marmosets, and perhaps other animal species. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

An Observational Investigation of Behavioral Contagion in Common Marmosets (Callithrix jacchus): Indications for Contagious Scent-Marking.

Behavioral contagion is suggested to promote group coordination that may facilitate activity transitions, increased vigilance, and state matching. Apart from contagious yawning, however, very little attention has been given to this phenomenon, and studies on contagious yawning in primates have so far only focused on Old World monkeys and apes. Here we studied behavioral contagion in common marmosets, a species for which group coordination and vigilance are paramount. In particular, we investigated the contagiousness of yawning, stretching, scratching, tongue protrusion, gnawing, and scent-marking. We coded these behaviors from 14 adult marmosets, from two different social groups. During testing sessions, animals were separated into groups of four individuals for 20-min observation periods, across three distinct diurnal time points (morning, midday, and afternoon) to test for circadian patterns. We observed almost no yawning (0.12 yawns/h) and very little stretching behavior. For all other behaviors, which were more common, we found several temporal and inter-individual differences (i.e., sex, age, dominance status) predictive of these responses. Moreover, we found that gnawing and scent-marking, which almost always co-occurred as a fixed-action pattern, were highly temporally clustered within observation sessions. We discuss the relative absence of yawning in marmosets as well as the possible function of contagious scent-marking, and provide suggestions for future research into the proximate and ultimate functions of these behaviors in marmosets.