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     

The communicative content of the common marmoset phee call during antiphonal calling

Vocalizations are a dominant means of communication for numerous species, including nonhuman primates. These acoustic signals are encoded with a rich array of information available to signal receivers that can be used to guide species‐typical behaviors. In this study, we examined the communicative content of common marmoset phee calls, the species‐typical long distance contact call, during antiphonal calling. This call type has a relatively stereotyped acoustic structure, consisting of a series of long tonal pulses. Analyses revealed that calls could be reliably classified based on the individual identity and social group of the caller. Our analyses did not, however, correctly classify phee calls recorded under different social contexts, although differences were evident along individual acoustic parameters. Further tests of antiphonal calling interactions showed that spontaneously produced phee calls differ from antiphonal phee calls in their peak and end frequency, which may be functionally significant. Overall, this study shows that the marmoset phee call has a rich communicative content encoded in its acoustic structure available to conspecifics during antiphonal calling exchanges. Am. J. Primatol. 72:974–980, 2010. © 2010 Wiley‐Liss, Inc.     

Contact calls of common marmosets (Callithrix jacchus): influence of age of caller on antiphonal calling and other vocal responses

Marmosets, as do many other primates, live in forest environments, are group living and constantly at risk of predation. Retaining contact with one another is therefore a matter of survival. We ask here whether their contact calls (phee and twitter vocalizations) are in some way ordered acoustically by sex or age and whether the calls of older marmosets elicit different responses than those of younger marmosets. In our study, marmosets (2–14 years) were visually isolated from conspecifics and the vocal responses to each isolated caller by other marmosets in the colony were recorded. Vocal responses to phee calls largely consisted of phee calls and, less commonly, twitter calls. No differences between the responses to calls by males and females were apparent. However, we found a strong positive and significant correlation between the caller's age and the percentage of its phee calls receiving a phee response, and a significant negative correlation between the caller's age and the percentage of its phee calls receiving a twitter response. The older the marmoset, the more antiphonal calling occurred. Two‐syllable phee calls were emitted more often by older marmosets (10–14 years) than by younger ones (2–6 years). Hence, we have found age‐dependent differences in phee‐call production and a consistent change in the response received across the adult life‐span. This age‐dependent effect was independent of kinship relations. This is the first evidence that marmosets distinguish age by vocal parameters alone and make social decisions based on age. Am. J. Primatol. 71:165–170, 2009. © 2008 Wiley‐Liss, Inc.     

Antiphonal call timing in marmosets is behaviorally significant: interactive playback experiments

Studies of primate vocal communication systems have generally focused on vocalizations and the information they convey to conspecifics. But the vocalizations are not the only sources of information. Aspects of each species vocal behaviors are likely to be communicatively rich as well. During vocal interactions, for example, the latency delay between the calls could communicate an important message to the signal receiver, such as an interest and willingness to socialize. Here we employed novel, interactive playback software to address this issue in the antiphonal calling behavior of common marmosets. In these experiments, we parametrically varied the latency delay of antiphonal call stimuli and measured its effects on subjects’ resultant vocal behavior. Results showed that marmosets produced successively fewer antiphonal call responses during test conditions with increasing latency delays. Moreover, although subjects produced significantly more antiphonal than spontaneous calls in conditions with antiphonal call timing delays up to 9 s, a longer delay resulted in a significant decline in calling. These data suggest that antiphonal call timing is a salient cue for maintaining antiphonal calling interactions and may be used by marmosets to determine whether a subsequent call is produced in response to or independently of their own.     

Within-session changes in licking as a function of sucrose concentration in common marmosets

Common marmosets (Callithrix jacchus) were allowed to lick sucrose solutions freely in 30-min sessions. We examined how the rate of licking changed in the course of a session and how the pattern of changes was affected by different concentrations (1%, 5%, and 25%) of solutions. The results showed that licking rates decreased monotonically regardless of the concentrations and that the decreasing patterns could be reasonably explained by exponential functions. The rates of decrease were slowest for the 5% solution and fastest for the 1% solution. The linear relation between the number of licks in a short interval and the cumulative number of licks before that interval, which was suggested by Aoyama (1996), did not always hold. The cumulative records of licking for individual sessions revealed that a break-and-run pattern of licking sometimes dominated after a licking rate slowed down, and that this pattern could disturb the linear relation.     

Time course of vocal modulation during isolation in common marmosets (Callithrix jacchus)

Common marmosets vocalize phee calls as isolation calls, which seem to facilitate their reunion with family groups. To identify multiple acoustic properties with different time courses, we examined acoustic modulations of phees during different social contexts of isolation. Subject marmosets were totally isolated in one condition, were visually isolated and could exchange vocalizations in another condition, and were visually isolated and subsequently totally isolated in a third condition. We recorded 6,035 phees of 10 male–female marmoset pairs and conducted acoustic analysis. The marmosets frequently vocalized phees that were temporally elongated and louder during isolation, with varying time courses of these changes in acoustic parameters. The vocal rates and sound levels of the phees increased as soon as the marmosets saw their pair mates being taken away, and then gradually calmed down. The phee duration was longer in conditions during which there were no vocal responses from their pair mates. Louder vocalizations are conspicuous and seem to be effective for long‐distance transmission, whereas shorter call duration during vocal exchanges might avoid possible vocal overlap between mates. Am. J. Primatol. 72:681–688, 2010. © 2010 Wiley‐Liss, Inc.     

Temporal rules in vocal exchanges of phees and trills in common marmosets (Callithrix jacchus)

Marmosets exchange two types of calls: phees and trills. We played back phees and trills to investigate the temporal rules of vocal exchanges using ten captive common marmosets (Callithrix jacchus). The marmosets usually emitted the same type of vocalizations just after the stimulus playbacks, and similar regularities were observed in the temporal intervals of phees and in trills. They vocalized with shorter intervals when they responded with trills rather than phees, and, after the first call, they repeatedly vocalized trills with shorter intervals than phees. These results suggest that the temporal rules between phees and trills are qualitatively similar but quantitatively different. These results might be owing to the different distances over which these contact calls are used. Am. J. Primatol. 71:617–622, 2009. © 2009 Wiley‐Liss, Inc.     

Whole blood transfusion in common marmosets: a clinical evaluation

In veterinary medicine, blood transfusion is commonly performed on companion animals. The common marmoset is a small nonhuman primate with increasing popularity as an animal model in biomedical research. Because of its small whole blood volume, the marmoset is at high risk of exsanguination, and blood transfusion is required to care for life-threatening bleeding. However, few clinical evaluations exist on transfusions for marmosets. This study performed whole blood transfusion with cross-matching on nine marmosets and surveyed the therapeutic effects. Recipients included clinical cases with persistent bleeding, anemia, and coma, as well as animals subjected to postoperative bleeding prophylaxis. Donors were selected from healthy marmosets, including littermates. Cross-match assay before transfusion were all negative, and recipients showed no visible signs of transfusion-related adverse reactions. Whole blood transfusions caused hemostasis and successful recovery in bleeding marmosets, including long-term improvement of anemia cases. Our results indicated that blood transfusion is effective for marmosets with severe anemia and persistent hemorrhage from both non-experimental and surgical causes. Furthermore, DNA sequencing for blood-group classification revealed that all subject marmosets were type A, suggesting that the risk of blood type mismatch may be low in this species.     

The behavioral context of visual displays in common marmosets (Callithrix jacchus)

Communication is important in social species, and may occur with the use of visual, olfactory or auditory signals. However, visual communication may be hampered in species that are arboreal have elaborate facial coloring and live in small groups. The common marmoset fits these criteria and may have limited visual communication. Nonetheless, some (contradictive) propositions concerning visual displays in the common marmoset have been made, yet quantitative data are lacking. The aim of this study was to assign a behavioral context to different visual displays using pre–post‐event‐analyses. Focal observations were conducted on 16 captive adult and sub‐adult marmosets in three different family groups. Based on behavioral elements with an unambiguous meaning, four different behavioral contexts were distinguished: aggression, fear, affiliation, and play behavior. Visual displays concerned behavior that included facial expressions, body postures, and pilo‐erection of the fur. Visual displays related to aggression, fear, and play/affiliation were consistent with the literature. We propose that the visual display “pilo‐erection tip of tail” is related to fear. Individuals receiving these fear signals showed a higher rate of affiliative behavior. This study indicates that several visual displays may provide cues or signals of particular social contexts. Since the three displays of fear elicited an affiliative response, they may communicate a request of anxiety reduction or signal an external referent. Concluding, common marmosets, despite being arboreal and living in small groups, use several visual displays to communicate with conspecifics and their facial coloration may not hamper, but actually promote the visibility of visual displays. Am. J. Primatol. 75:1084–1095, 2013. © 2013 The Authors. American Journal of Primatology Published by Wiley Periodicals, Inc.     

Body mass growth in common marmosets: Toward a model of pediatric obesity

While much is known about adult obesity in nonhuman primates, very little is known regarding development of childhood adiposity. As small monkeys that are easy to handle and have a relatively fast life history, common marmoset monkeys (Callithrix jacchus) offer interesting opportunities to examine the question of fat versus lean mass growth in a nonhuman primate. This article provides an overview of our understanding of early life growth in mass in marmoset monkeys, based primarily upon our past 20 years of research, culminating in our recent findings on early life obesity in this species. Common marmosets display variance in early life growth patterns that is related to both pre‐ and postnatal factors and the marmoset uterine environment is exquisitely designed to reflect resources available for the gestation of multiple offspring, making them an interesting model of developmental programming. We have demonstrated that obesity can be generated in very early life in captive marmosets, with excess adiposity evident by one month of age, making this species a potentially valuable model in which to study pediatric obesity and its sequelae. Birth weight is associated with adiposity in animals vulnerable to obesity. Early life exposure to higher fat diets enhances the chances of postweaning obesity development. However, overall higher food consumption is also associated with obesity development at later ages. One unexpected finding in our studies has been the relatively high body fat percentage of neonatal (12–18%) marmosets suggesting that hypotheses regarding the uniqueness of high human neonatal adiposity merit further examination. Am J Phys Anthropol, 2013. © 2012 Wiley Periodicals, Inc.     

Social influences on the development of foraging behavior in free-living common marmosets (Callithrix jacchus)

In this study we investigated the extent and pattern of social influences (i.e., the use of a conspecific as a model) on the foraging behavior of immature, wild common marmosets (Callithrix jacchus) as a function of the age of individuals. We compared the foraging activities and interactions with subadult and adult group members (older than 15 months) of young infants (1-2 months old), older infants (3-4 months old), and juveniles (5-10 months old). In addition to measuring the intensities of model-independent foraging (MIF) and merely paying attention to the model's foraging activities, we examined the frequencies of three types of model-dependent foraging (MDF): "follow the model", "manipulate the same object", and "forage together". We found that older infants were the most attentive and most socially-influenced foragers among the three age categories in absolute terms, but were not more attentive than young infants given their low foraging activity. Juveniles, in contrast, tended to have reduced overall foraging intensity compared to infants, but showed relatively more MDF in cases in which they observed subadult or adult models. Female models appeared to be more attractive than male models. These findings suggest that infants are generally more attentive to the foraging behavior of subadults and adults than juveniles, with the latter being more influenced when they had observed a model before. These subtle age-dependent effects of social foraging not only extend the assumption that young primates seek information from adults, they also suggest a complex interplay among physical and cognitive maturation, independence, and social dynamics.     

From social behavior to neural circuitry: steroid hormones rapidly modulate advertisement calling via a vocal pattern generator

Across vertebrates, androgens are rapidly elevated within minutes in response to aggressive or reproductive stimuli, yet it is unclear what the causal relationship is between fast androgen elevation and the ongoing (minute-by-minute) expression of behavior. This study tested the hypothesis that rapid increases in plasma steroid levels induce similarly rapid increases in both vocal behavior and the neurophysiological output of a central pattern generator that governs vocal behavior. In Gulf toadfish (Opsanus beta), males call to attract females to their nesting sites, and both males and females vocalize in aggressive interactions. Previous field experiments with males showed that simulated territorial challenges produce rapid and concurrent elevations in ongoing calling behavior and circulating levels of the teleost-specific androgen 11-ketotestosterone (11kT), but not the glucocorticoid cortisol. The current field experiments showed that non-invasive (food) delivery of 11kT, but not cortisol, induced an elevation within 10 min in the ongoing calling behavior of males. Electrophysiological experiments revealed that intramuscular injections of either 11kT or cortisol, but neither testosterone nor 17-beta-estradiol, induced increases within 5 min in the output of the vocal pattern generator in males, whereas only cortisol had similarly fast effects in females. The field behavioral results support predictions generated by the challenge hypothesis and also parallel the 11kT-dependent modulation of the vocal pattern generator in males. The cortisol effect on the vocal pattern generator in both sexes predicts that glucocorticoids regulate vocalizations in non-advertisement contexts. Together, these experiments provide strong support for the hypothesis that surges in circulating steroid levels play a causal role in shaping rapid changes in social behavior (vocalizations) through non-genomic-like actions on neural (vocal motor) circuits that directly encode behavioral patterning.     

Exploratory behavior and learning in laboratory marmosets (Callithrix jacchus jacchus): Comparisons between experimental-cage and home-cage activity

In this paper I examine exploratory behavior and learning in two groups of common marmosets (Callithrix jacchus jacchus), both living under laboratory conditions. The main aim of my studies was to compare behavior occurring in an experimental testing situation with home-cage behavior, and to assess conditions under which exploration is enhanced. One group of marmosets was tested individually in an experimental room away from a larger animal holding room, and a second group was observed in their own home cages, surrounded by other marmosets. Marmosets in both groups were given the opportunity to learn simple tasks, such as pressing a lever for food or jumping on to a wire grid to open a door and see a neighbouring marmoset, and were provided with sets of novel or familiar objects to encourage play and exploration. In the isolated experimental cage, marmosets which learnt a lever-pressing task showed higher general activity levels than controls; in the home cages the mere addition of novel objects resulted in enhancements in exploratory behavior (measured in terms of contacts with the objects). Although the activities associated with learning tended to decline over time, the novel objects remained a constant interest throughout the experiment. The results have implications for maintaining marmosets in captivity, especially in situations when they are housed separately.     

Hormonal changes related to paternal and alloparental care in common marmosets (Callithrix jacchus)

The physiological mechanisms of parental and alloparental care in cooperatively breeding nonhuman primate species such as the common marmoset (Callithrix jacchus) are poorly known. In this study, we examined prolactin and cortisol plasma levels of fathers and older offspring of both sexes, with and without previous experience in infant carrying, around parturition and during infant carrying. Blood samples were collected from fathers and older offspring and prolactin and cortisol were measured by RIA and EIA, respectively. Prolactin levels of both caretakers were not influenced by infant's birth, previous experience or proximity to parturition. However, prolactin levels increased in both caretakers while in physical contact with infants and also with the number of infants being carried in older offspring. These findings suggest that increased prolactin seems to be mainly due to physical effort rather than a physiological trigger of paternal and alloparental care in common marmosets. Cortisol levels were higher for experienced fathers shortly before parturition which could act to reinforce affiliative bonds between breeding males and females at this time or in the ability of males to detect the proximity of the parturition or both.     

Long-term study of infant-carrying behavior in captive common marmosets (Callithrix jacchus): Effect of nonreproductive helpers on the parents' carrying performance

Infant-carrying behavior in four families ofCallithrix jacchus was investigated over a period covering six to eight litters. We evaluated the effect of the total number of helpers and the number of adult helpers on the parents' carrying performance for the total carrying period and for three age stages of the infants. The carrying performance of the parents reached an asymptote beginning with litters 3 to 5. In two groups, the carrying performance of the parents was significantly negatively correlated with group size. However, considerable differences existed within each group and between the groups. The mother was the primary caregiver in the early weeks of the infants' lives. In this phase the helpers' contribution to carrying was less than might be expected. The relief of the parents from infant-carrying was greatest when the infants were 4 to 7 weeks old. Breeding males benefited most and from every helper, while breeding females benefited most from adult helpers, i.e., the carrying performance of the breeding female was considerably reduced until the respective group had grown to 8 to 10 members (infants not included). This group size is considered to be ideal for maximal relief of the parents from infant carrying. An increasing number of adult nonreproductive helpers (>4 or 5) does not induce a further reduction of the parents' carrying performance. Infant-rearing experience of nonreproductive helpers seems to be more important for the parents' and, especially, the breeding female's relief from infant-carrying than the overall number of helpers is. The data also strongly evidence that a group member's participation in infant-carrying is influenced by housing conditions and the demographic history of the group.     

Collagen-induced arthritis in common marmosets: a new nonhuman primate model for chronic arthritis

Introduction  

There is an ever-increasing need for animal models to evaluate efficacy and safety of new therapeutics in the field of rheumatoid arthritis (RA). Particularly for the early preclinical evaluation of human-specific biologicals targeting the progressive phase of the disease, there is a need for relevant animal models. In response to this requirement we set out to develop a model of collagen-induced arthritis (CIA) in a small-sized nonhuman primate species (300 to 400 g at adult age); that is, the common marmoset (Callithrix jacchus).