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.     

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.     

Mobbing vocalizations as a coping response in the common marmoset

Using a non-invasive method of sampling saliva followed by assay for cortisol levels, we found that common marmosets (Callithrix jacchus) show a decrease in cortisol levels after seeing a snake-model stimulus that reliably elicits mobbing (tsik) calls. In fact, there was a significant positive correlation between the number of tsik vocalizations made and the magnitude of the decrease in the cortisol concentrations. Furthermore, marmosets with higher levels of cortisol prior to being exposed to the stimulus produce more tsik calls than those with lower levels of cortisol. Subsequent experiments showed that, in response to 15 min of isolation with no visual or auditory contact with conspecifics (a traditional stressor), cortisol levels increased significantly. However, playback of the mobbing calls of a familiar conspecific to individual isolated marmosets not only prevented the rise in cortisol, but also actually caused a decrease in the levels of this hormone. This suggests that the mobbing calls serve to calm the marmoset after experiencing a stressful situation. This finding results in a greater understanding as to the role of physiological responses during communication in this species and could have implications for the welfare of marmosets in captivity.     

Production and perception of sex differences in vocalizations of Wied's black‐tufted‐ear marmosets (Callithrix kuhlii)

Males and females from many species produce distinct acoustic variations of functionally identical call types. Social behavior may be primed by sex‐specific variation in acoustic features of calls. We present a series of acoustic analyses and playback experiments as methods for investigating this subject. Acoustic parameters of phee calls produced by Wied's black‐tufted‐ear marmosets (Callithrix kuhlii) were analyzed for sex differences. Discriminant function analyses showed that calls contained sufficient acoustic variation to predict the sex of the caller. Several frequency variables differed significantly between the sexes. Natural and synthesized calls were presented to male–female pairs. Calls elicited differential behavioral responses based on the sex of the caller. Marmosets became significantly more vigilant following the playback of male phee calls (both natural and synthetic) than following female phee calls. In a second playback experiment, synthesized calls were modified by independently manipulating three parameters that were known to differ between the sexes (low‐, peak‐, and end‐frequency). When end‐frequency‐modified calls were presented, responsiveness was differentiable by sex of caller but did not differ from responses to natural calls. This suggests that marmosets did not use end‐frequency to determine the sex of the caller. Manipulation of peak‐and low‐frequency parameters eliminated the discrete behavioral responses to male and female calls. Together, these parameters may be important features that encode for the sex‐specific signal. Recognition of sex by acoustic cues seems to be a multivariate process that depends on the congruency of acoustic features. Am. J. Primatol. 71:324–332, 2009. © 2008 Wiley‐Liss, Inc.     

Changes In Rhesus Macaque 'Coo' Vocalizations during Early Development

In order to test whether ‘coo’ calls of young rhesus macaques, Macaca mulatta, undergo some modifications during early development, and to explore which factors may influence these changes, we studied the ontogeny of their contact call, the ‘coo’ call. Vocalizations were recorded during brief periods of social separation. Infants were either raised with their mothers and other conspecifics, or separated from their mothers at birth and housed in a nursery with other infants. We recorded calls uttered in the separation context from 20 infants. We digitized the first 50 calls of a given series and subjected them to a Fourier transform. From each frequency–time spectrum, we extracted 65 acoustic parameters using a software program (LMA 5.9). We then used a cluster analysis to separate the ‘coo’ calls from other call types. With increasing age, the ‘coos’ dropped in pitch and became more even. The course of amplitude became more constant and the call duration increased slightly. Nevertheless, we found a high intra‐individual variation throughout the 5 mo. Neither rearing condition nor sex had any apparent influence on age‐related changes in ‘coo’ structure. With one exception, all parameters that correlated with age could be explained by variation in weight. Therefore, we conclude that growth is the main factor accounting for the observed changes.     

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.     

Sex hormone influence on human infants' sound characteristics: melody in spontaneous crying

The specific impact of sex hormones on brain development and acoustic communication is known from animal models. Sex steroid hormones secreted during early development play an essential role in hemispheric organization and the functional lateralization of the brain, e.g. language. In animals, these hormones are well-known regulators of vocal motor behaviour. Here, the association between melody properties of infants'' sounds and serum concentrations of sex steroids was investigated. Spontaneous crying was sampled in 18 healthy infants, averaging two samples taken at four and eight weeks, respectively. Blood samples were taken within a day of the crying samples. The fundamental frequency contour (melody) was analysed quantitatively and the infants'' frequency modulation skills expressed by a melody complexity index (MCI). These skills provide prosodic primitives for later language. A hierarchical, multiple regression approach revealed a significant, robust relationship between the individual MCIs and the unbound, bioactive fraction of oestradiol at four weeks as well as with the four-to-eight-week difference in androstenedione. No robust relationship was found between the MCI and testosterone. Our findings suggest that oestradiol may have effects on the development and function of the auditory–vocal system in human infants that are as powerful as those in vocal-learning animals.     

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.     

Innate development of acoustic signals for host parent–offspring recognition in the brood‐parasitic Screaming Cowbird Molothrus rufoaxillaris

Young birds communicate their need to parents through complex begging displays that include visual and acoustic cues. Nestlings of interspecific brood parasites must ‘tune’ into these communication channels to secure parental care from their hosts. Various studies show that parasitic nestlings can effectively manipulate host parental behaviour through their begging calls, but how these manipulative acoustic signals develop in growing parasites remains poorly understood. We investigated the influence of social experience on begging call development in a host‐specialist brood parasite, the Screaming Cowbird Molothrus rufoaxillaris. Screaming Cowbird nestlings look and sound similar to those of the primary host, the Greyish Baywing Agelaioides badius. This resemblance is likely to be adaptive because Baywings discriminate against fledglings unlike their own and provision nests at higher rates in response to Baywing‐like begging calls than to non‐mimetic begging calls. By means of cross‐fostering and playback experiments, we tested whether the acoustic cues that elicit recognition by Baywings develop innately in Screaming Cowbird nestlings or are acquired through social experience with host parents or nest mates. Our results suggest that begging call structure was partially modulated by experience because Baywing‐reared Screaming Cowbird and host nestlings were acoustically more similar as age increased, whereas acoustic similarity between cross‐fostered and Baywing‐reared Screaming Cowbird nestlings decreased from 4–5 to 8–10 days of age. Cross‐fostered Screaming Cowbirds developed begging calls of lower minimum frequency and broader bandwidth than those of Baywing‐reared Screaming Cowbirds by the age of 8–10 days. Despite the observed differences in begging call structure, however, adult Baywings responded similarly to begging calls of 8‐ to 10‐day‐old cross‐fostered and Baywing‐reared Screaming Cowbirds, suggesting that these were functionally equivalent from the host's perspective. These findings support the idea that, although rearing environment can influence certain begging call parameters, the acoustic cues that serve for offspring recognition by Baywings develop in young Screaming Cowbirds independently of social experience.     

Environmental correlates of vocal communication of wild pygmy marmosets, Cebuella pygmaea

We quantified the acoustic characteristics of the habitats of two wild populations of pygmy marmosets, in Amazonian Ecuador to evaluate their effects on vocal signal structure. We obtained measures of ambient noise, sound attenuation and reverberation through recordings and broadcasts of exemplars of two short-range vocalizations and one long-range vocalization of the marmosets. Ambient noise levels differed among habitats. The calls of pygmy marmosets had frequencies that coincided with relatively quiet regions of the ambient noise spectra of the habitats. The three vocalization types were degraded similarly in all habitats. The two short-range signals, with a pulsatile structure, were more affected by reverberation than was the long-range, less pulsatile vocalization. This degradation could be used by the marmosets to estimate the distance of the caller animals. We obtained data on context of vocalizations from six groups of pygmy marmosets, three from each population, in both the dry and rainy seasons. The use of Trills, J calls and Long calls was related to the distance between the calling animal and the potential receivers suggesting that marmosets are using the calls in a way appropriate to the effects of habitat acoustics. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Mother-Infant Communication in the Lesser Spear-nosed Bat Phyllostomus discolor (Chiroptera,Phyllostomidae) — Evidence for Acoustic Learning

When mother-offspring couples of Phyllostomus discolor (lesser spear-nosed bat) are reunited after separation, an intensive exchange of infants' isolation calls and mothers' directive calls can be observed. The directive calls of each mother show a distinctive frequency-time structure, which appears to represent her individual vocal signature. During ontogenesis the isolation calls of the young change gradually, adapting increasingly to the mother's call type. A comparison of calls of separated pups at different ages with their mothers' directives demonstrated the individually distinct call characteristics of the mother also to be characteristic of the isolation calls of her young by about 50 days of age. This suggests that acoustic signals may be learned in Phyllostomus discolor.     

Optimisation of the transmit beam parameters for generation of subharmonic signals in native and altered populations of a commercial microbubble contrast agent SonoVue®

The aim of this work was to establish the optimum acoustic characterisation approach and insonation transmit beam parameters for subharmonic signal generation with ‘native’ and ‘altered’ populations of a commonly-used microbubble contrast agent. Dynamic contrast-enhanced (DCE) ultrasound is a non-invasive method of imaging the microvasculature, typically implemented using harmonic imaging. Subharmonic imaging, in which echoes at half the fundamental frequency are detected, detects signals which are generated by the ultrasound contrast agents (UCAs) but not by tissue. However, optimal transmission parameters and furthermore, the optimum acoustic characterisation method have not been established. The subharmonic response of ‘native’ and ‘altered’ UCA, altered through decantation, was investigated at transmit centre frequencies 1.8–5 MHz and pulse lengths 1–8 cycles. The ‘altered’ UCA had reduced polydispersity (1–4 µm: 82% bubble volume), compared to ‘native’ (4–10 µm: 57% bubble volume). A custom-built narrow-band acoustic characterisation system was found to be more appropriate for acoustic characterisation compared to the commonly used broadband pulse-echo approach. Both UCA generated the highest subharmonic signal at pulse length of 3-cycles. The maximum ‘native’ subharmonic signal was generated at a transmit centre frequency of 1.9 MHz, corresponding to a subharmonic at 0.95 MHz. This optimal frequency increased in the ‘altered’ population to 2.3–2.5 MHz, bringing the subharmonic above 1 MHz and hence into a range amenable to clinical abdominal imaging transducers. The use of subharmonic signal detection coupled with a modified UCA size distribution has potential to significantly improve the quantification sensitivity and accuracy of DCE ultrasound imaging.     

A continental assessment of diurnality in frog calling behaviour

Acoustic signalling is evolutionarily important, influencing sexual selection and serving as a premating isolation mechanism. There is a strong evolutionary basis for acoustic signalling to occur nocturnally across many terrestrial vertebrate groups including mammals, reptiles and amphibians. Within some of these groups, there is a general assumption that ‘most taxa are nocturnal’ in their acoustic signalling, and this is a particularly strongly held view for most frogs. Here we challenge this well-accepted notion by quantifying diurnal calling behaviour in Australian frogs, leveraging a continental-wide citizen science dataset. Of 196 species present in the citizen science dataset, 140 (71%) were recorded at least once during the day. Of the most commonly observed species (i.e. species with at least 150 calls recorded in the database), there were surprisingly high rates of diurnal calling: 14 species had >25% of their calls recorded during the day. We also found that the relative rate of diurnal calling in frogs showed a strong phylogenetic signal, suggesting that the plasticity in calling behaviour as it relates to time of the day is strongly evolutionarily conserved. Our results highlight a suite of ecological and evolutionary questions that are worthy of further investigation.     

Post-natal growth, mother-infant interactions and development of vocalizations in the vespertilionid bat Plecotus auritus

Female brown long-eared bats Plecotus auritus nurse their own young selectively. Choice experiments suggested that females recognized infants by using both olfactory and acoustic cues. Infant isolation calls (i-calls) showed individual variation, and vocal signatures allowed the females to recognize and suckle their own pup. As the pups grew, the i-calls increased in frequency and decreased in duration, and the i-calls appeared to change into orientation cries. Mothers were able to recognize recent calls of their own babies in preference to older calls. Echolocation sounds were distinguishable statistically between lactating females, and the behaviour of the babies during choice experiments suggested that in this species a mutual acoustic recognition occurs. The growth and development of wing shape in P. auritus are described.     

Long‐distance call evolution in the Felidae: effects of body weight,habitat, and phylogeny

Long‐distance calls used for mate attraction and territorial spacing are distinctive signals in the felid vocal repertoire. Their evolution is subject to natural and sexual selection, as well as various constraints. Body size is an important morphological constraint, with the scaling of the spectral characteristics of a species' vocalizations with its body size being established for several vertebrate groups. Alternatively, the structure of long‐distance calls may have been optimized for transmission in species' habitats (acoustic adaptation hypothesis). The present study assessed whether the mean dominant frequency of long‐distance calls in the Felidae (approximately 70% of all species incorporated) is influenced by the species' body size and/or conforms to the acoustic adaptation hypothesis. After controlling for phylogenetic relationships, we found a significant correlation between mean dominant frequency of a taxon's long‐distance calls and conditions for sound transmission in its habitat type (‘open/heterogeneous’ versus ‘dense’), although no significant influence of body size. Taxa living in more open habitat types have long‐distance calls with significantly lower mean dominant frequencies than those living in dense habitats. The result obtained in the present analysis is fairly robust against random removal of single or few taxa from the data, and also against the use of different branch‐length transformation models in phylogenetic regression. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 487–500.     

Context and sex differences exist in the acoustic structure of phee calls by newly–paired common marmosets (Callithrix jacchus)

Captive common marmosets of all ages robustly produce a “separation” phee call during brief separations from their group. In contrast, a second structural variant, which may function as an intergroup call, is produced in the home cage primarily by the reproductive adults. A previous study found that postpubertal but nonreproductive offspring rarely produce phee calls when in the home cage with the natal group, yet these marmosets call frequently after pairing with an opposite‐sex partner. The sudden increase in home cage phee calls may indicate the rapid onset of intergroup calling. Alternatively, marmosets may be producing the separation phee variant as a result of separation from the natal group. The present study investigated whether phee calls produced by recently paired individuals in the home cage were structurally distinguishable from their calls recorded in a separation paradigm. We also tested whether sex differences, known to exist in the calls of mature adults, could be found in calls recorded from younger, nonreproductive animals separated from their natal groups. We analyzed 18 acoustic parameters of phee calls produced in the home cage after pairing and of calls produced during separation both from the natal group and from a new mate. Discriminant function analyses found that home cage calls were clearly discriminable from separation calls (average 91.7% correctly classified), indicating that the rapid increase in home cage phee call production shortly after pairing is not a consequence of separation from the family group. Postpubertal marmosets appear to show a rapid behavioral adjustment to separation from their natal groups. Additionally, sex was clearly discriminable in calls recorded both before and after pairing (average 86.8% correctly classified). Like calls recorded from well‐established paired marmosets, phee calls produced by recently paired, postpubertal marmosets are discriminable by context and sex. Am. J. Primatol. 49:165–181, 1999. Published 1999 Wiley‐Liss, Inc.     

COO TYPES IN THE COLLARED DOVE STREPTOPELIA DECAOCTO: ONE THEME,DISTINCTIVE VARIATIONS

ABSTRACT

Dove coos are known to be important for intra-specific communication in various contexts. Earlier research showed the occurrence of systematic frequency modulations for the perch- coo of the collared dove and suggested that presence or absence of these modulations might be important in communication. The present study examined the occurrence of frequency modulations and frequency use for perch-, bow- and nest-coo, as well as variation in these features between and within individuals, to assess the acoustic ‘signal space’ for this species. The occurrence of frequency modulations was high for perch- and bow-coo, but low for the nest-coo. The relative distribution of modulations over the three elements of a coo differed for the various coo types. Coo types differed also in their ‘frequency profiles’. Frequency use is correlated with the occurrence of modulations. Differences between coo- types as well as variation within a coo-type and within individuals can be described by a limited set of parameters, which may be linked to basic properties of the coo producing mechanism. As a consequence of the occurrence of modulations and their distribution over the coo-types, the acoustic differences between the coo-types are amplified. As the different coo-types serve different functions, presence of modulations increases the signal space and decreases the ambiguity of the coo types. Differences between individuals exceeded those within individuals and were largest for perch- and bow-coo, which both serve in territorial defence and mate attraction.     

BOOK REVIEW

Echolocation calls of four species of insectivorous bats of central Chile were recorded and characterized to determine vocal signatures that allow their identification in the field. Pulses of Tadarida brasiliensis were characterized by the highest duration and the lowest values for all frequencies, which do not overlap those of the remaining species. Tadarida emits narrowband, shallow frequency-modulated search calls. All three vespertilionid species studied (Histiotus montanus, Lasiurus varius and Myotis chiloensis) showed similar echolocation design to one another, consisting of a downward frequency modulation at the beginning of the signal followed by a narrowband quasi-constant frequency component; however, their calls differ by their spectral characteristics. Discriminant function analysis of six acoustic parameters (duration, initial frequency, slope frequency modulation, peak frequency, minimal and maximal frequencies) gave an overall classification of 87.4%, suggesting species could be correctly classified based on echolocation calls. Call duration and minimal frequency were the variables most important for species identification.     

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.

     

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.