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.     

Social context affects phee call production by nonreproductive common marmosets (Callithrix jacchus)

Common marmosets produce two variants of their long call (phee call) in different situations. Intergroup calls are produced in territorial situations, and intragroup separation calls are produced by marmosets isolated from group members. Marmoset groups frequently include postpubertal, nonreproductive members; their roles in the spontaneous production of territorial vocalizations is unclear. This study analyzed the production of home cage phee calls by nonreproductive, postpubertal marmosets while they were housed in their natal groups and after pairing with an opposite-sex conspecific. Additionally, the production of the separation phee call variant was assessed in both social conditions. The results indicated that the marmosets rarely produced home cage, or territorial, phee calls while they were natally housed. In contrast, both males and females produced the territorial phee call at a much higher rate as early as 4 days after pairing. Age-matched females remaining in their natal groups throughout the study produced home cage phee calls infrequently. Most marmosets produced separation phee calls at a high rate after separation from either their natal group or a partner, suggesting that the makeup of a social group has little effect on an animal's motivation to reunite with conspecifics. These results suggest that the social environment has an important influence on the production of territorial phee calls. Am. J. Primatol. 43:135–146, 1997. © 1997 Wiley-Liss, Inc.     

Syntactical Organization of the Gargle Vocalization of the Black-capped Chickadee,Parus atricapillus

The gargle is a complex call of the black-capped chickadee Parus atricapillus associated with agonistic interactions. A large sample of calls was recorded from five sites in southeastern Wisconsin. Three sites were near one another and the other two with a different dialect pattern were more distant (all sites were within 15 km of each other). A typical call consists of about 6 notes selected from an array of about 15 different note-types that are shared among individuals in the same population. Note-types are given in many combinations, and any individual may deliver many different variations. Analysis of two- and three-note sequences shows a syntactical organization with certain note-types much more likely to precede or follow than others. In some cases linkage between note-types was nearly complete. Some differences occurred among individuals and sites, but general organizational rules were similar. One effect on ordering was acoustical structure of the notes. Higher pitched, shorter duration notes were more likely at the beginning than the end of the call which often consisted of trills. Organization of the gargle was compared to that of the chick-a-dee call of the same species. Similarities include recombinant properties, general acoustic rules and syntax. A major difference may be that in chick-a-dee calls various note combinations constituting a call have different meanings, while the various note combinations comprising an individual's repertoire of gargles may be functionally equivalent.     

Neural function of the mesencephalic dorsomedial nucleus (DM) on distance call production in Bengalese finches

In sexually mature Bengalese finches, acoustic structures of distance calls show sexual difference. The dorsomedial nucleus (DM) of intercollicular complex is known as the midbrain vocal center of distance calls. Neural input from the robust nucleus of archistriatum (RA) was observed in the DM of sexually mature males, but not observed in that of sexually mature females. The purpose of this study is to clarify somo more details of physiological function of the neural system in the DM in distance call production. Electrical stimulation to the DM of both sexes induced a call acoustically similar to distance calls, whose duration depended on the number of the pulses/train of electrical stimulation; electrical stimulation in relatively large (or small) numbers of pulses/train induced calls with relatively long (or short) duration, respectively. Multi-unit spikes were recorded from neurons in the DM. The increment of the frequency of recorded spikos was large when the bird vocalized distance calls, and the number of the frequency decreased when the bird vocalized calls whose duration was shorter than that of distance calls. These results suggest that the neural system in the DM controls duration of distance calls in sexually mature males and females. Electrical stimulation to the DM under different pulse frequencies induced calls with different patterns of time-frequency characteristics. The relation between the pulse frequencies and time-frequency characteristics showed sexual difference. The relation between them in RA-lesioned males was similar to that in females. These results suggest that the neural circuit in the DM of sexually mature males is consisted of sexually common neural circuit controlled by the neural input from the RA, and that these sexually different neural system produce sexually different acoustic structures of distance calls.     

Social Change Affects Vocal Structure in a Callitrichid Primate (Callithrix kuhlii)

Vocal plasticity in the face of changing social context is well‐documented in passerine birds, but the degree to which changes in social environment affect the vocal structure of non‐human primates is a topic which has remained largely unexplored. We assessed whether modification of social environments, in this case the presence of marmosets in neighboring cages, influenced the vocal morphology of phee calls, which possess ‘signature’‐like features, in Wied's black tufted‐ear marmosets (Callithrix kuhlii). Individual phee calls were obtained over a period of 8 wk from 11 animals maintained in rooms with stable social environments. After this baseline phase, seven marmosets were housed for an additional 8 wk in rooms that contained cages with unfamiliar marmosets, while four marmosets maintained the same neighbors as the first phase. Calls were digitized and both frequency and temporal parameters were measured. Multivariate discriminant function analyses (DFA) generated from vocalizations collected in the first phase produced functions that accurately classified calls to the correct individual, showing that calls had significant individual distinctiveness. DFAs generated from vocalizations in the first phase of the study continued to show high classification accuracy for marmosets in a stable social environment, but DFAs from the first phase were significantly less likely to correctly classify vocalizations in marmosets that were housed next to novel conspecifics. These data show that phee calls, which have signature‐like properties in marmosets, can be modified by changes in social context. The results suggest a degree of plasticity in vocal signals that is rare among non‐human primates.     

Individuality but not Stability in Marmoset Long Calls

Individually distinct communication signals (‘signatures’) have been documented in a variety of taxa across signal modalities and they serve a host of important functions. However, studies have rarely examined the temporal stability of these signals. Cooperatively breeding species, such as marmosets and tamarins, are characterized by long-term group membership, complex social organization, and high levels of interindividual coordination of behaviour. These social attributes may promote complex, individually distinct and stable acoustic signals to facilitate the expression of cooperative behaviour. In this study, the long calls of socially housed individual Wied's black tufted-ear marmosets, Callithrix kuhli, were examined for a ‘signature system’ potentially important in such interactions. Vocalizations were recorded at three different times (1993, 1995, 1996), digitized, and then measured by spectrographic analysis. Acoustic and temporal features of the calls were examined, including number of syllables, length of syllables, intersyllable interval, frequency range, start/stop frequency, peak frequency, and total call duration. A number of significant intra-individual changes in acoustic parameters were identified across the recording periods. Discriminant analysis revealed that many variables contributed to differentiation among individuals, and average classification accuracy for calls within a given year was high, ranging from 91.7% to 93.5%. However, reclassification accuracy for calls between-years was much poorer, averaging less than 50%. In addition, classification confidence was higher for within-year scores in contrast to the between-year values. Thus, tufted-ear marmosets have an individually distinct vocalization which is acoustically modified across time. Our finding suggests that to the extent that the vocalization is used for individual recognition, recognition mechanisms must be modified over time as well.     

Responses to natural and synthetic phee calls by common marmosets (Callithrix jacchus)

Captive adult common marmosets (Callithrix jacchus) produce whistlelike “phee” calls in two contexts: in the home cage, where phee calls may function as part of territorial marking behavior, and when separated from social companions, where phee calls may function to reunite conspecifics. Natural and synthesized calls representing the acoustic structure of male and female calls in each context were presented to adult marmosets in a playback paradigm. Marmosets demonstrated discriminative abilities according to the context of the call and the caller's sex. Vocal and behavioral responses indicated increased vigilance and territorial behavior, following playbacks of naturally produced calls as well as synthetic calls. All animals scanned more frequently following produced calls as well as synthetic calls. All animals scanned more frequently following natural home cage as well as isolation calls, but only increased contact behavior (trills) in response to home cage calls. The responses were dimorphic according to the sex of the caller, where adult males scanned more following male calls, and adult females were more aggressive following male and female calls. The differential behavioral responses to playbacks of marmoset phee calls suggest a biological relevance to subtle differences found in the acoustic parameters of the phee call. © 1994 Wiley-Liss, Inc.

1 This article is a US Government work and, as such, in the public domain in the United States of America.

     

Degree of social contact affects the emission of food calls in the common marmoset (Callithrix jacchus)

The aim of this study was to investigate whether the emission of food calls in common marmosets (Callithrix jacchus) is influenced by different social contexts. Food calls are emitted by this species only in the presence of preferred food. If these calls have any communicative function, it may be that individuals produce food calls in order to call family mates toward the food source. If this is the case, the number of calls produced should vary in accordance with the number of family mates present at the moment of the discovery of the food, i.e., the fewer family mates nearby, the more food calls are emitted. This hypothesis was tested with five pairs of common marmosets, by recording the number of food calls emitted in four experimental conditions: 1). isolation: completely isolated from the family mates; 2). visual isolation: separated by a wooden panel from the family mates; 3). visual contact: separated by a wire-mesh from the family mates; and 4). physical interaction: together with the family mates. The results show that the proportion of intervals during which food calls were produced by the pairs was significantly different in the four experimental conditions. It decreased from the isolation and visual isolation condition, through the visual contact condition, reaching the lowest value in the physical interaction condition. The variation observed in the proportion of intervals during which food calls were emitted, in relation to different social contexts, is an indication in favor of the communicative function of this vocalization.     

Vocalizations of Belding's ground squirrels (Spermophilus beldingi)

Vocalizations of Belding's ground squirrels (Spermophilus beldingi) were recorded during the summer of 1982 near Tioga Pass in the central Sierra Nevada of California. Sonagrams were made and call parameters were measured. Discriminant function analyses revealed that multiple-note calls (‘trills’) differed acoustically depending on whether they occurred in response to a predator, or were given by males following copulations. The post-copulatory trills of males were individually distinctive. Among anti-predator trills there was no evidence of predator-specificity within the narrow range of predators tested: trills given to two species of (stuffed) weasels (Mustela), to dogs and to humans were statistically indistinguishable. Sonagrams of trills occurring in agonistic contexts suggest that a third general category of trills may exist, but agonistic trills were more variable than either anti-predator or post-copulatory trills. The ground squirrels also gave single-note calls in the three contexts described above, either repetitively (‘chirps’) or singly (‘whistles’). Neither chirps nor whistles encoded any obvious situation-specific information, except that whistles were typically associated with rapidly-moving predators, usually raptors. The post-copulatory chirps of males were individually distinctive. Vocalizations of Belding's ground squirrels may not vary among contexts as much as do the analogous calls of California ground squirrels (S. beecheyi).     

Stability and change in the vocal signatures of common marmoset mobbing calls

Alarm calls that carry information about the identity of the caller may help the receiver decide how to react. We recorded the tsik calls of six captive adult marmosets (Callithrix jacchus) in two different social groups in response to snake models at two time points (summer 2014 and January 2015). We measured eight acoustic variables including duration, inter-call interval, minimum and maximum frequency, and starting, maximum and ending peak frequency. Discriminant function analyses (DFA) confirmed that calls were individually distinct at both time periods (78.88 and 79.89% correctly classified at time one and time two, respectively). Stability of the vocal signatures was assessed using the DFA model for summer 2014 to classify calls elicited in January 2015. Although the classification rates were lower in 2015, calls were still classified more than would be expected by chance (64.50%). This suggests that acoustic signatures of common marmoset tsik calls remain fairly stable over time and therefore remain recognizable by their groupmates. However, during that six-month period, at least three (out of seven) acoustic parameters changed such that they were significantly higher or lower in all six marmosets; in two marmosets six out of seven parameters changed. Changes to individual ‘voices’ of animals, despite overall stability reflected in above-chance matching of calls over time in a DFA analysis, may have implications for acoustic research.     

Comparing Contact Calling Between Black Tufted-Ear Marmosets (<Emphasis Type="Italic">Callithrix penicillata</Emphasis>) in a Noisy Urban Environment and in a Quiet Forest

All habitats have some level of noise but anthropogenic sounds such as those produced by traffic are structurally different from natural sounds, and could cause organisms living in noisy urban areas to modify their vocal communication. We compared temporal and spectral parameters of contact calls in black tufted-ear marmosets (Callithrix penicillata) living in a noisy and a quiet area. From February 2009 to March 2012 we recorded spontaneously produced phee vocalizations by marmosets in two areas in Minas Gerais, Brazil: a noisy urban park (N = 581) in Belo Horizonte, and a quiet natural forest, on Cauaia farm in Matozinhos city (N = 560). We measured the duration, frequencies, and rate of phee vocalizations. We found that marmosets’ phee vocalizations were significantly longer in the noisy area than in the quiet area. The low, high, and dominant frequencies were significantly lower in the noisy area than in the quiet area, and contact calling was less frequent in the noisy area than in the quiet area. We suggest that the differences between marmoset contact calls from noisy and quiet areas are influenced by anthropogenic noise.     

Contexts and behavioral correlates of trill vocalizations in wild white-faced capuchin monkeys (Cebus capucinus)

Primate vocalizations that appear to occur independently of specific contexts typically are considered to be contact calls. However, results from several recent studies indicate that these calls function to facilitate social interactions. White-faced capuchin monkeys (Cebus capucinus) emit a high-frequency vocalization, termed a "trill," in social interactions and during travel. In this study, immatures emitted most trills, but adult females also trilled; by contrast, adult males rarely trilled. Infants emitted the majority of trills, and they trilled at significantly higher rates than adult females. Infants trilled most when approaching other individuals. Furthermore, infants emitted proportionately more trills than other age classes when approaching other individuals. I therefore focused on the detailed context and immediate behavioral correlates of trilling by infants. Infants that trilled when approaching others tended to interact affiliatively with them subsequently (i.e., climbing on, touching, receiving grooming, and performing food inspection) more than infants that did not trill when approaching. Therefore, infant trilling may have had an immediate effect on the recipient's behavior.     

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.     

Pygmy Marmosets Modify Call Structure When Paired

Pygmy marmosets ( Cebuella pygmaea ) modified the structure of their trill vocalizations in response to pairing with a new mate. Prior to pairing, individual marmosets displayed different acoustic parameters of trill structure. Within the first 6 wk after pairing, three of four pairs produced trills that were more homogeneous between mates. Pairs that had the greatest individual difference in trill structure prior to pairing displayed convergence on a greater number of parameters than pairs having fewer differences in prepairing trill structure. The vocal structure following pairing remained highly stable in the two pairs that could be recorded 3 yr after initial pairing. Changes in trill structure that occurred within the first 6 wk after pairing were greater than spontaneous changes that occurred during baseline control recording sessions on the same animals. These results suggest that nonhuman primates show subtle modification of vocal structure, especially in response to changes in social environment. Similar findings have been reported in birds and other mammals.     

Dialects in pygmy marmosets? Population variation in call structure

Population variation in primate vocal structure has been rarely observed. Here, we report significant population differences in the structure of two vocalizations in wild pygmy marmosets (Trills and J calls). We studied 14 groups of pygmy marmosets Callithrix (Cebuella) pygmaea pygmaea from five populations in northeastern Ecuador. We analyzed the acoustic structure of Trills and J calls recorded from two adult animals in each group through focal samples. Although individuals and groups within a population differed in call structure, we found consistent structural differences at a population level for Trills and J calls. Pair‐wise comparisons for the two call types point to San Pablo and Amazoonico as the populations that differed the most, whereas Hormiga and Zancudococha showed the least differences. Discriminant function analysis indicates that calls from each population could be classified accurately at rates significantly above chance. Habitat acoustics, social factors and genetic drift may explain interpopulation vocal differences. This is the first evidence of within‐subspecies vocal differences, or dialects, in wild populations of a neotropical primate species. Am. J. Primatol. 71:333–342, 2009. © 2009 Wiley‐Liss, Inc.     

Field Cricket Species Differences in the Temporal Patterns of Long-Distance Mate Attraction Signals

We quantify variation in the temporal components of long‐distance mate attraction signals produced by a North American field cricket, Gryllus rubens Scudder. Total signaling time, trilling bout duration, and hourly bout number exhibit high repeatability within individuals. Extensive variation exists across individuals: some males never signal while others signal for several hours each night; of the signalers, average trilling bout duration ranges from <1 min to well over an hour; some males produce only one trilling bout in an evening while others produce three bouts every 2 h. Body size, weight, wing morphology, and condition do not appear to explain the variation. We compare the temporal signaling components of G. rubens with its sister species, G. texensis. Although G. rubens produce slightly more trills per hour with slightly shorter trilling bout durations, the temporal components of these long‐distance mate attraction signals are surprisingly similar across species.     

Visual scanning by common marmosets (Callithrix jacchus): Functional aspects and the specialrrole of adult males

The rates of visual scanning and vocalizations were studied in a group of captive marmosets (Callinthrix jacchus) after the presentation of five different stimuli (artificial flower, playback of long calls, female/male conspecific, stuffed wild cat) in order to assess the function of visual scanning. Only the presentation of a stuffed cat induced a significant response. The adult males in particular increased their scanning rate and all adult individuals decreased their rate of vocalizations. The results indicate that visual scanning in marmosets is an appropriate measure of vigilance which seems to serve the function of predator detection and avoidance. The strong response of adult males suggests that they play a special role in predator detection.     

Individual recognition of contact calls by pygmy marmosets

Individual recognition by voice has been frequently assumed to be an important phenomenon in the social species. The present study on pygmy marmosets (Cebuella pygmaea) demonstrated that there are distinctive acoustic features in each of two contact calls by which individuals could be distinguished from each other. Individual pygmy marmosets responded differently depending on which type of contact call was given and on the identity of the vocalizing animal. Playbacks of individual calls through hidden speakers produced some evidence for differential individual responses, but only when they originated from familiar locations. These results indicate that pygmy marmosets recognize each other on the basis of their contact calls.     

Food transfers in wild and reintroduced golden lion tamarins,Leontopithecus rosalia

We collected data from wild and reintroduced golden lion tamarins (Leontopithecus rosalia) to describe the behavior of donor and recipient during food transfers, evaluate the effect of supplemental feeding on food transfer behavior, and examine various hypotheses concerning the function of food transfers in primates. Behavioral observations were conducted on 12 groups of tamarins with young (N = 30) between the ages of 1 week and 1 year old. Results show that food transfers involve various behaviors, from steals by recipients to offers by donors; transfers mostly derive from adults and are directed at immature weaned young (between 3 and 9 months old); and that most items transferred were prey or fruits that require skill to process. Eleven percent of food transfers were preceded by an adult vocalization specific to that context, whereas 86% were preceded by conspicuous infant vocalizations and begging behavior. The most common vocalizations were loud and atonal (rasps) and broad banded frequency modulated (trills). Infants born to reintroduced parents vocalized less, whereas reintroduced adults vocalized more before transferring food than their wild counterparts. Reintroduced adults and young received more food transfers (4.4 per hr) than did wild‐born adults and young (2.2 per hr). Our findings suggest that food transfer in golden lion tamarins is best understood as provisioning of young that have not fully developed foraging skills to ensure they get the necessary resources for growth and survival. Am. J. Primatol. 48:305–320, 1999. © 1999 Wiley‐Liss, Inc.