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.     

Use of male blue monkey “Pyow” calls for long-term individual identification

This study examines whether individual adult male blue monkeys (Cercopithecus mitis stuhlmanni) can be identified through acoustic analysis of their “pyow” calls. It is possible to reliably assign the pyow call of the blue monkeys of Kibale Forest, Uganda, to the individual caller based on the acoustic properties of the vocalization. Analysis of pyows made by a recognizable male over a 10-yr period shows that the acoustic properties of one individual's pyow call can remain relatively constant over time. Acoustic analysis of pyow calls may provide a relatively easy and reliable method to document tenure lengths of adult male blue monkeys resident in groups. Similar analyses of the loud calls of other species of primates may, likewise, prove to be useful in documenting long-term membership. © 1992 Wiley-Liss, Inc.     

Social Factors Influence the Acoustic Variability in the Long-distance Calls of Male Chimpanzees

Acoustic variability in the species-typical long-distance calls of male chimpanzees was investigated. Analysis of 13 acoustic features revealed that calls varied more within than between individuals. Although only a limited amount of acoustic variability was attributable to different populations, discriminant-function analysis confirmed that males from two populations produce acoustically distinguishable calls. Additional investigation suggested that social factors may contribute to the patterns of acoustic variation both between and within individuals. Matrix-permutation tests revealed a positive association between the amount of time males spent together and a measure of call similarity. Vocal similarities between individuals appeared to result from a dynamic process involving chorusing behaviour: males matched the acoustic characteristics of each other's vocalizations when calling together. Chorusing may also affect the degree of within-individual acoustic variation in calls. Males who chorused often with others produced more variable calls than individuals who chorused less often or called alone.     

Call type signals caller goal: a new take on ultimate and proximate influences in vocal production

After 40 years of debate it remains unclear whether signallers produce vocalizations in order to provide receivers with information about call context or external stimuli. This has led some researchers to propose that call production is arousal‐ or affect‐based. Although arousal influences certain acoustic parameters within a call type, we argue that it cannot explain why individuals across vertebrates produce different call types. Given emerging evidence that calls are goal‐based, we argue that call type is a signal of a caller's goal to elicit a change in receiver behaviour. Using chimpanzees (Pan troglodytes) and vervet monkeys (Cercopithecus aethiops) as case studies, we demonstrate the two benefits of viewing call production as signalling both caller goal (which determines call type) and caller arousal (which affects within‐call‐type variation). Such a framework can explain first, why a single class of calls is apparently given in multiple contexts, and, second, why some species have larger call repertoires than others. Previous studies have noted links between sociality and repertoire size, but have not specified exactly why animals living in societies that are more complex might require a greater number of differentiated signals. The caller‐goal framework potentially clarifies how social complexity might favour call diversification. As social complexity increases, callers may need to elicit a larger number of distinct behaviours from a wider range of distinct audiences.     

Vocal repertoire of cooperatively breeding Smooth‐billed Anis

Calls are functionally diverse signals that mediate behavior in a wide variety of contexts in both passerines and non‐passerines. However, the call‐based acoustic communication systems of non‐passerines have received less attention from investigators than those of passerines. We examined the vocal repertoire of Smooth‐billed Anis (Crotophaga ani), cooperatively breeding cuckoos that live in groups with multiple breeding pairs. We recorded calls from 22 groups over two breeding seasons at the Cabo Rojo National Wildlife Refuge in Puerto Rico. We identified 11 call types and one group vocalization, and used an automated sound measurement program to quantify their acoustic features. Discriminant function analysis (DFA) correctly classified 74.2% of calls based on these features. The vocal repertoire of Smooth‐billed Anis is larger than that reported for the three other species in the subfamily Crotophaginae. Smooth‐billed Anis have at least two alarm calls, two nest‐specific calls, and one nest defense call. We also identified one possible signal of aggressive intent, one possible appeasement signal, and two calls that may communicate identity. The relatively large vocal repertoire of Smooth‐billed Anis and association of distinct call types with different functions and contexts supports the main prediction of the social complexity hypothesis, i.e., species with more complex social systems will have more complex communication systems.     

A comparison of individual distinctiveness in three vocalizations of the dwarf mongoose (Helogale parvula)

Individual specificity can be found in the vocalizations of many avian and mammalian species. However, it is often difficult to determine whether these vocal cues to identity rise from “unselected” individual differences in vocal morphology or whether they have been accentuated by selection for the purposes of advertising caller identity. By comparing the level of acoustic individuality of different vocalizations within the repertoire of a single species, it is possible to ascertain whether selection for individual recognition has modified the vocal cues to identity in particular contexts. We used discriminant function analyses to determine the level of accuracy with which calls could be classified to the correct individual caller, for three dwarf mongoose (Helogale parvula) vocalizations: contact, snake, and isolation calls. These calls were similar in acoustic structure but divergent in context and function. We found that all three call types showed individual specificity but levels varied with call type (increasing from snake to contact to isolation call). The individual distinctiveness of each call type appeared to be directly related to the degree of benefit that signalers were likely to accrue from advertising their identity within that call context. We conclude that dwarf mongoose signalers have undergone selection to facilitate vocal individual recognition, particularly in relation to the species’ isolation call.     

Social and vocal behavior in adult greater tube-nosed bats (Murina leucogaster)

Many studies have revealed the significant influence of the social nature and ecological niche of a species on the design and complexity of their communication sounds. The knowledge of communication sounds and particularly of the flexibility in their use among mammals, however, remains patchy. Being highly vocal and social, bats are well suited for investigating vocal plasticity as well as vocal diversity. Thus, the overall aim of this study was to test the presence of structural overlap between calls used in social communication and echolocation pulses emitted during foraging in greater tube-nosed bats (Murina leucogaster). Acoustic analysis and spectrotemporal decomposition of calls revealed a rich communication repertoire comprising 12 simple syllables and 5 composites with harmonics in the ultrasonic range. Simultaneous recording of vocal and social behavior in the same species yielded a strong correspondence between distinct behaviors and specific call types in support of Morton's motivation-structure hypothesis. Spectrographic analysis of call types also revealed the presence of modified components of echolocation pulses embedded within social calls. Altogether, the data suggest that bats can parse complex sounds into structurally simpler components that are recombined within behaviorally meaningful and multifunctional contexts.     

Social Correlates of Variation in Male Calling Behavior in Blanchard's Cricket Frog,Acris crepitans blanchardi

I studied variation in male calling behavior and its social correlates in Blanchard's cricket frog, Acris crepitans blanchardi. Calls were produced in distinct call groups, and they increased in duration and complexity from the beginning to end of a call group. Dominant frequency was the only character of 18 quantified consistently correlated with male snout-vent length. Calls from the beginning of a call group varied independently of calls from the middle and end of a call group, and only calls from the beginning of a call group exhibited significant variation among males, thus relative consistency within males. Other characters varied greatly within individual males. Unlike most other anurans, dominant frequency also exhibited tremendous within-male variation. The relative influence of caller density, local caller density, nearest neighbor distance, and nearest neighbor sound pressure level on variation in male calling behavior was examined. Nearest neighbor distance, mediated through the sound-pressure level of neighbor calls, appeared to have the greatest influence on variation in male calling behavior. The most profound changes in calling behavior occurred during aggressive encounters; males altered their calling behavior in a manner suggesting that they respond to competitors with graded aggressive signals. Furthermore, the structure of the communication system suggests that calls are graded not only in response to the level of social competition, but graded over a call group as well.     

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.     

The Structure of Bonobo Copulation Calls During Reproductive and Non‐Reproductive Sex

Copulation calls in primates are usually identified as sexually selected signals that promote the reproductive success of the caller. In this study, we investigated the acoustic structure of copulation calls in bonobos (Pan paniscus), a great ape known for its heightened socio‐sexuality. Throughout their cycles, females engage in sexual relations with both males and other females and produce copulation calls with both partners. We found that calls produced during sexual interactions with male and female partners could not be reliably distinguished in terms of their acoustic structure, despite major differences in mating behaviour and social context. Call structure was equally unaffected by the size of a female’s sexual swelling and by the rank of her mating partner. Rank of the partner did affect call delivery although only with male, but not female partners. The only strong effect on call structure was because of caller identity, suggesting that these signals primarily function to broadcast individual identity during sexual interactions. This primarily social use of an evolved reproductive signal is consistent with a broader trend seen in this species, namely a transition of sexual behaviour to social functions.     

Variation in pika (Ochotona collaris,O. princeps) vocalizations within and between populations

Understanding geographic call variation can resolve evolutionary and behavioural questions, yet the factors influencing divergent acoustic signals remain poorly understood in mammals. We explored call variation between collared pikas in Yukon and Alaska and American pikas in Alberta, and between individuals within a population of collared pikas. Classification trees were used to determine the extent of call divergence between populations and the elements of calls driving these differences. Pika populations had significant differences in call structure, and individual pikas were classified to their correct populations with up to 94% accuracy. To investigate possible mechanisms responsible for interspecific variability, we tested the acoustic adaptation hypothesis by using a playback experiment to explore whether American and collared pika calls transmit with less degradation across their own species' habitat than the habitat of their congener. We found no support for the acoustic adaptation hypothesis. Geographic call variation in these two species of pikas likely reflects genetic divergence, and may be a result of separate evolutionary histories. We calculated the potential for individual coding for both time and frequency measurements of calls. High frequency harmonics showed greater between‐ than within‐individual variation, and may act as sources of information regarding individual identity.     

Sources of Acoustic Variation in Rhesus Macaque (Macaca mulatta))Vocalizations

All species in the genus Macaca produce a set of harmonically rich vocalizations known as “coos”. Extensive acoustic variation occurs within this call type, a large proportion of which is thought to be associated with different social contexts such as mother-infant separation and the discovery of food. Prior studies of these calls have not taken into account the potential contributions of individual differences and changes in emotional or motivational state. To understand the function of a call and the perceptual salience of different acoustic features, however, it is important to determine the different sources of acoustic variation. I present data on the rhesus macaques' (M. mulatta) coo vocalization and attempt to establish some of the causes of acoustic variation. A large proportion of the variation observed was due to differences between individuals and to putative changes in arousal, not to differences in social context. Specifically, results from a discriminant-function analysis indicated that coo exemplars were accurately assigned to the appropriate individual, but vocal “signatures” were more variable in some contexts than in others. Moreover, vocal signatures may not always be reliable cues to caller identity because closely related individuals sound alike. Rhesus macaque coos evidently provide sufficient acoustic information for individual recognition and possibly kin recognition, but are unlikely to provide sufficient information about an external referent.     

Males’ calls carry information about individual identity and morphological characteristics of the caller in burrowing petrels

Acoustic communication in burrowing petrels has been poorly studied. However, as for many other bird species, acoustic communication seems to play an essential role in social interactions during the breeding season of these seabirds. Bachelor males call from their burrow, likely to attract females, but also when vocally challenged by other males. Calling in the breeding colony exposes petrels to high predation risks and thus it should provide an important benefit. The present study focuses on the informative content of males’ calls in the blue petrel Halobaena caerulea and the Antarctic prion Pachyptila desolata, two monogamous petrel species producing a single egg per year. We tested the hypotheses that acoustic parameters of a male's calls 1) reflect phenotypic characteristics, and 2) bear an individual vocal signature. To do so, we first tested on both species the relationships between seven morphometric measurements and 11 acoustic parameters using multivariate analyses. Second, we performed a between‐class analysis and calculated the potential of individuality coding (i.e. the ratio between intra‐ and inter‐individual variabilities) for acoustic parameters in both spectral and temporal domains. Results show acoustic parameters (especially energy quartiles, call duration, and syllable or phrase rate) reflect the caller's body size, bill morphology and wing morphology in both species. Considering the seeming pertinence of wing morphology, we suggest wing area may be a more relevant trait to consider than wing length when studying soaring birds. The results support the idea that energy quartiles, phrase rate and call duration also code for individual identity. Information carried by males’ calls might play a role in social interactions, such as burrow defence (e.g. male‐male competition, neighbour‐stranger discrimination) and/or female mate choice.     

Little Brown Bats (Myotis lucifugus) Recognize Individual Identity of Conspecifics Using Sonar Calls

Bats use sonar calls to locate prey and orient in their environment but they may also be used by conspecifics to obtain information about a caller. Statistical analysis of sonar calls provides evidence that variation carries social information about a caller, including individual identity. We hypothesized that little brown bats (Myotis lucifugus) would be able to recognize individuals given the potential fitness benefits of doing so. We performed playback trials using a habituation‐discrimination design to determine whether little brown bats are able to recognize the individual identity of a caller based on variation in their sonar calls. Each subject bat was played the calls of bat A until they habituated (defined as a 50% decrease from the beginning call rate), then the calls of bat B or a new call sequence of bat A (a control, referred to as bat A’) were played. Each subject received a unique pair of playback recordings (bat A and B) from adult female bats from the same colony (but a different colony from the subject) and the order of trials was randomized. The response measures were habituation time (s) and call rate (calls/s). Within a trial, subjects habituated to calls of bat A and transferred this habituation to the bat A’ sequence. In addition, they increased their call rates when played calls of bat B. Comparing between trials, subjects increased their call rate to the calls of bat B to a greater relative extent than to the calls of bat A’. These results provide the first evidence that bats recognize individual identity of conspecifics (as opposed to discrimination of groups), which has implications for the social interactions of bats.     

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.     

Situational Specificity in Alpine-marmot Alarm Communication

We studied the degree to which alpine marmot (Marmota marmota L.) alarm calls function as communication about specific external stimuli. Alpine marmots emit variable alarm calls when they encounter humans, dogs, and several species of aerial predators. The first part of the study involved observations and manipulations designed to document contextual variation in alarm calls. Alarm calls varied along several acoustic parameters, but only along one that we examined, the number of notes per call, was significantly correlated with the type of external stimulus. Marmots were more likely to emit single-note alarm calls as their first or only call in response to an aerial stimulus, and multiple-note alarm calls when first calling to a terrestrial stimulus. This relationship was not without exceptions; there was considerable variation in the number of notes they emitted to both aerial and terrestrial stimuli, and a single stimulus type — humans — elicited a wide range of acoustic responses. The second part of the study involved playing back three types of alarm calls to marmots and observing their responses. Marmots did not have overtly different responses to the three types of played-back alarm calls. Our results are consistent with the hypotheses that: 1. Alarm calls do not refer to specific external stimuli; 2. Alarm calls function to communicate the degree of risk a caller experiences; and 3. Alarm calls require additional contextual cues to be properly interpreted by conspecifics.     

Who is Calling? Intraspecific Call Variation in the Aromobatid Frog Allobates femoralis

Many territorial species respond less aggressively to familiar neighbours than to unfamiliar floating strangers based on individual differences in acoustic signals. This form of social recognition, termed neighbour–stranger discrimination (NSD) or dear-enemy phenomenon has been reported so far from three anuran species. To investigate the potential of auditory signal features to convey information on sender's identity, we determined patterns of within-male and between-male variability in the advertisement call of the aromobatid frog Allobates femoralis . We examined 285 calls from 19 males to assess those call properties showing sufficient and reliable inter-individual differences to function as possible recognition cues. Beside calls per call bout and call rate, all other examined call properties were more variable among males than within males. Generally, temporal call features showed higher between- and within-male variability ratios than spectral properties and contributed mostly to distinguish individual males in the discriminant-function analysis. Mean classification success of 64.9% correctly assigned calls to individual males is mainly attributable to three temporal call properties (duration of note 1 and 4, note repetition rate). Altogether, our results suggest that there is sufficient variation in the advertisement call to discriminate statistically among individual males. However, assessed call differences between A. femoralis males were rather small, suggesting that potential NSD might be based either on a combination of call features or even on the whole pattern of individual call variation instead on single call properties. Habituation–discrimination experiments in the field using modified playback signals to test for differential behavioural responses are required to confirm this hypothesis.     

Variability in spider monkeys' vocalizations may provide basis for individual recognition

Analysis of long-range vocalizations given by spider monkeys revealed consistent acoustic differences among the calls of individuals. Of seven acoustic measurements, four exhibited significant variation between individuals. A discriminant analysis demonstrated that two of these variables allowed correct identification of the caller 44% of the time. Including the remainder of the variables increased the percentage correctly identified to 50%. Individual identification by call structure could benefit spider monkeys, where individuals forage separately in subgroups and the interactions between specific pairs of individuals is highly variable. Acoustic recognition of callers would facilitate the choice of which subgroups to join, thus allowing individuals to manipulate the size and composition of their subgroups. In addition, the calls of mothers and offspring appeared to be similar in acoustic properties.     

The Vocal Repertoire of Barbary Macaques: A Quantitative Analysis of a Graded Signal System

The vocal behavior of Barbary macaques (Macaca sylvanus) was studied in an outdoor enclosure at Rocamadour, France. Ad libitum recordings were made across a broad array of socioecological contexts from 92 individually identified subjects from all age—sex classes. From the recordings, 8479 calls were sampled and submitted to a Fourier transform. A custom software program was used to determine 35 acoustic parameters describing the call in terms of its frequency and time dynamics. On these parameters a cluster analysis was used to examine the acoustic morphology of the Barbary macaque vocal repertoire. The analysis revealed a highly graded structure with intergraded variations between different clusters (‘call types’). There were clear age-related preferences in usage of different clusters, but animals of all ages were potentially able to produce the whole array of call types. The major sex difference was a differential use of certain call types in specific situations. Despite a clear sex dimorphism in body size no significant sex differences in the acoustic structure of calls in adults was found. There were no unidirectional relationships between the acoustic structure of a call and the context in which it was uttered, although call usage was more specific in some contexts than in others. The results suggest that the major factor underlying the variation in acoustic structure reflect the internal state of the caller.