Individual variation in pup vocalizations and absence of behavioral signs of maternal vocal recognition in Weddell seals (Leptonychotes weddellii)

Individually stereotyped vocalizations often play an important role in relocation of offspring in gregarious breeders. In phocids, mothers often alternate between foraging at sea and attending their pup. Pup calls are individually distinctive in various phocid species. However, experimental evidence for maternal recognition is rare. In this study, we recorded Weddell seal (Leptonychotes weddellii) pup vocalizations at two whelping patches in Atka Bay, Antarctica, and explored individual vocal variation based on eight vocal parameters. Overall, 58% of calls were correctly classified according to individual. For males (n= 12) and females (n= 9), respectively, nine and seven individuals were correctly identified based on vocal parameters. To investigate whether mothers respond differently to calls of familiar vs. unfamiliar pups, we conducted playback experiments with 21 mothers. Maternal responses did not differ between playbacks of own, familiar, and unfamiliar pup calls. We suggest that Weddell seal pup calls may need to contain only a critical amount of individually distinct information because mothers and pups use a combination of sensory modalities for identification. However, it cannot be excluded that pup developmental factors and differing environmental factors between colonies affect pup acoustic behavior and the role of acoustic cues in the relocation process.     

Does vocal learning accelerate acoustic diversification? Evolution of contact calls in Neotropical parrots

Learning has been traditionally thought to accelerate the evolutionary change of behavioural traits. We evaluated the evolutionary rate of learned vocalizations and the interplay of morphology and ecology in the evolution of these signals. We examined contact calls of 51 species of Neotropical parrots from the tribe Arini. Parrots are ideal subjects due to their wide range of body sizes and habitats, and their open‐ended vocal learning that allows them to modify their calls throughout life. We estimated the evolutionary rate of acoustic parameters of parrot contact calls and compared them to those of morphological traits and habitat. We also evaluated the effect of body mass, bill length, vegetation density and species interactions on acoustic parameters of contact calls while controlling for phylogeny. Evolutionary rates of acoustic parameters did not differ from those of our predictor variables except for spectral entropy, which had a significantly slower rate of evolution. We found support for correlated evolution of call duration, and fundamental and peak frequencies with body mass, and of fundamental frequency with bill length. The degree of sympatry between species did not have a significant effect on acoustic parameters. Our results suggest that parrot contact calls, which are learned acoustic signals, show evolutionary rates similar to those of morphological traits. This is the first study to our knowledge to provide evidence that change through cultural evolution does not necessarily accelerate the evolutionary rate of traits acquired through life‐long vocal learning.     

Sex identification in King Penguins Aptenodytes patagonicus through morphological and acoustic cues

In the context of sexual selection, animals have developed a variety of cues conveying information about the sex of an individual to conspecifics. In many colonial seabird species, where females and males are monomorphic and do not show obvious differences in external morphology, acoustic cues are an important signal for individual and sex recognition. Here, we study the vocal and morphological sex dimorphism in the King Penguin Aptenodytes patagonicus, a colonial, monomorphic seabird for which our knowledge about the role of vocalizations and morphology in mate choice is very limited. Data were collected at Possession Island, Crozet Archipelago, in a breeding colony consisting of about 16 000 breeding pairs. Using measurements of six morphological features and analysing acoustic parameters of call recordings of adult individuals, we show that King Penguins can be sexed based on a single morphological measurement of the beak with an accuracy of 79%. We found a sex‐specific syntax in adult King Penguin calls that provided a 100% accurate method to distinguish between the sexes in our study population. To confirm the method at the species level, we analysed calls recorded from King Penguin adults in Kerguelen Island, 1300 km away from our study population and found the same accuracy of the sex‐specific syntax. This sex‐specific syllable arrangement is rare in non‐passerines and is a first step in understanding the mate choice process in this species. Furthermore, it offers a cost‐effective, non‐invasive technique for researchers to sex King Penguins in the field.     

Vocal Repertoire of Cebus capucinus: Acoustic Structure, Context, and Usage

Researchers studying nonhuman primate vocal repertoires suggest that convergent environmental, social, and motivational factors account for intra- and interspecific vocal variation. We provide a detailed overview of the vocal repertoire of white-faced capuchins, including acoustic analyses and contextual information of vocal production and vocal usage by different age-sex classes in social interactions. The repertoire is a mixture of graded and discrete vocalizations. In addition, there is general support for structural variation in vocalizations with changes in arousal level. We also identified several combined vocalizations, which might represent variable underlying motivations. Lastly, by including data on the social contexts and production of vocalizations by different age-sex classes, we provide preliminary information about the function of vocalizations in social interactions for individuals of different rank, age, and sex. Future studies are necessary to explore the function of combined vocalizations and how the social function of vocalizations relate to their acoustic structure, because social use of vocalizations may play an important role in shaping vocal evolution.     

Geographic variation in the calls of wild chimpanzees: A reassessment

Male chimpanzees produce a species‐typical call, the pant hoot, to communicate to conspecifics over long‐distances. Calls given by males from the well‐known Gombe and Mahale populations typically consist of four different phases: an introduction, build‐up, climax, and let‐down. Recent observations suggest that chimpanzees living in the Kibale National Park, Uganda, consistently give calls that lack a build‐up and are thus qualitatively distinguishable acoustically from those made by other East African conspecifics. We analyzed additional recordings from Mahale and Kibale to re‐examine geographic variation in chimpanzee calls. Results indicate that males from both sites produce pant hoots containing all four parts of the call. Calls made by chimpanzees from the two populations, however, differ in quantitative acoustic measures. Specifically, males at Kibale initiate their calls with significantly longer elements and build‐up over briefer periods at slower rates than individuals from Mahale. Kibale males also deliver acoustically less variable calls than chimpanzees at Mahale. Although climax elements do not differ between populations in any single acoustic feature, discriminant function analysis reveals that acoustic variables can be used in combination to assign calls to the correct population at rates higher than that expected by chance. Ecological factors related to differences in habitat acoustics, the sound environment of the local biota, and body size are likely to account for these observed macrogeographic variations in chimpanzee calls. Am. J. Primatol. 47:133–151, 1999. © 1999 Wiley‐Liss, Inc.     

Bat echolocation calls facilitate social communication

Bat echolocation is primarily used for orientation and foraging but also holds great potential for social communication. The communicative function of echolocation calls is still largely unstudied, especially in the wild. Eavesdropping on vocal signatures encoding social information in echolocation calls has not, to our knowledge, been studied in free-living bats so far. We analysed echolocation calls of the polygynous bat Saccopteryx bilineata and found pronounced vocal signatures encoding sex and individual identity. We showed experimentally that free-living males discriminate approaching male and female conspecifics solely based on their echolocation calls. Males always produced aggressive vocalizations when hearing male echolocation calls and courtship vocalizations when hearing female echolocation calls; hence, they responded with complex social vocalizations in the appropriate social context. Our study demonstrates that social information encoded in bat echolocation calls plays a crucial and hitherto underestimated role for eavesdropping conspecifics and thus facilitates social communication in a highly mobile nocturnal mammal.     

The acoustic expression of stress in a songbird: Does corticosterone drive isolation-induced modifications of zebra finch calls?

Animal vocalizations convey multiple pieces of information about the sender. Some of them are stable, such as identity or sex, but others are labile like the emotional or motivational state. Only a few studies have examined the acoustic expression of emotional state in non-human animals and related vocal cues to physiological parameters. In this paper, we examined the vocal expression of isolation-induced stress in a songbird, the zebra finch (Taeniopygia guttata). Although songbirds use acoustic communication extensively, nothing is known to date on how they might encode physiological states in their vocalizations. We tested the hypothesis that social isolation in zebra finches induces a rise of plasma corticosterone that modifies the vocal behavior. We monitored plasma corticosterone, as well as call rate and acoustic structure of calls of males in response to the playback of female calls of varied saliences (familiar versus stranger) in two situations: social isolation and social housing. Social isolation induced both a rise in plasma corticosterone, and a range of modifications in males' vocal behavior. Isolated birds showed a lower vocal activity, an abolition of the difference of response between the two stimuli, and evoked calls with longer duration and higher pitch. Because some of these effects were mimicked after oral administration of corticosterone in socially housed subjects, we conclude that corticosterone could be partly responsible for the isolation-related modifications of calls in male zebra finches. To our knowledge, this is the first demonstration of the direct implication of glucocorticoids in the modulation of the structure of vocal sounds.     

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.     

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.     

Chimpanzees Extract Social Information from Agonistic Screams

Chimpanzee (Pan troglodytes) agonistic screams are graded vocal signals that are produced in a context-specific manner. Screams given by aggressors and victims can be discriminated based on their acoustic structure but the mechanisms of listener comprehension of these calls are currently unknown. In this study, we show that chimpanzees extract social information from these vocal signals that, combined with their more general social knowledge, enables them to understand the nature of out-of-sight social interactions. In playback experiments, we broadcast congruent and incongruent sequences of agonistic calls and monitored the response of bystanders. Congruent sequences were in accordance with existing social dominance relations; incongruent ones violated them. Subjects looked significantly longer at incongruent sequences, despite them being acoustically less salient (fewer call types from fewer individuals) than congruent ones. We concluded that chimpanzees categorised an apparently simple acoustic signal into victim and aggressor screams and used pragmatics to form inferences about third-party interactions they could not see.     

Selection for acoustic individuality within the vocal repertoire of wild chimpanzees

Individual primates typically produce acoustically distinct calls. To investigate the factors that facilitate the evolution of individual vocal signatures, we examined two components of the call repertoire of chimpanzees: the pant hoot and pant grunt. Pant hoots are long-distance signals whose recipients can be several hundred meters away, while pant grunts are short-range calls given to conspecifics within close visual range. Given their markedly different contexts of emission, we predicted that natural selection would favor the elaboration of individually distinctive acoustic features in pant hoots compared with pant grunts. Analyses of nine acoustic features revealed that pant hoots are more stereotyped within-individuals and variable between-individuals than pant grunts. These data are consistent with the hypothesis that selection may act to encode varying degrees of individuality in different components of the vocal repertoire of a single species.     

Acoustic convergence and divergence in two sympatric burrowing nocturnal seabirds

Shearwaters are nocturnal burrowing seabirds. They return to their colony at dusk and exhibit high vocal activity, underlining the usefulness of acoustic cues to nocturnal communication. The present study aimed to test whether acoustic communication systems of two sympatric shearwater species, the Yelkouan shearwater Puffinus yelkouan and the Mediterranean Cory's shearwater Calonectris diomedea diomedea , converge to similar strategies. Inter-annual mate fidelity and incubation relays led us to focus on sex and individual acoustic signatures. We first characterized those two signatures by analysing the major call emitted by incubating birds. Second, we performed playback experiments to assess ability of birds to vocally discriminate between sexes and mate versus non-mate. The results obtained show that both species use a reliable sex vocal signature supported by frequency and energy features, enabling sex identification of the emitter. By responding only to conspecific same-sex calls, birds may ensure burrow and mate guarding. Conversely, individual vocal signature was mainly supported by temporal parameters, and was more reliable in the Cory's shearwater. Moreover, this species uses vocal exchanges to identify the mate during incubation relays, whereas Yelkouan shearwaters probably need additional cues. In conclusion, we observe an evolutionary convergence in intra-sex communication process but a divergence in mate greeting strategy.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 115–134.     

Mother-lamb acoustic recognition in sheep: a frequency coding

Ewes of the domestic sheep ( Ovis aries ) display selective maternal investment by restricting care to their own offspring and rejecting alien young. This trait relies on individual recognition processes between ewes and lambs. Whereas identification at the udder is only olfactory, distance recognition is performed through visual and acoustic cues. We studied the effectiveness and modalities of mutual acoustic recognition between ewes and lambs by spectrographic analysis of their vocal signatures and by playbacks of modified calls in the field. Our results show that ewes and their lambs can recognize each other based solely on their calls. The coding of identity within the vocal signatures, previously unknown in sheep, is similar in lamb and ewe: it uses the mean frequency and the spectral energy distribution of the call, namely the timbre of the call. These results point out a simple signature system in sheep that uses only the frequency domain. This engenders a signal with low information content, as opposed to some highly social birds and mammal species that may integrate information both in the temporal and spectral domains. The simplicity of this system is linked to the roles played by vision and olfaction that corroborate the information brought by the vocal signature.     

Spectrographic Description of Vocalizations in Captive Otolemur garnettii

To advance knowledge of the vocal communication associated with close proximity social interactions in Garnett's greater bush baby (Otolemur garnettii), we measured acoustic and temporal properties of vocalizations from videotaped recordings of captives in two main social contexts: mother-infant interactions and adult male-female pair introductions and reintroductions. We used a real-time sonagraph or software program to display, edit, and analyze vocal waveforms, and to provide wideband and narrowband spectrograms. Vocalization characteristics measured include fundamental frequency (via inspection of harmonics) and spectral features such as formant frequency, intensity, and duration. The vocal repertoire contained 4 major types of vocalizations: 1) barks and complex multiple bark sequences, 2) low frequency flutter/hums and growls, 3) high frequency clicks and spits, and 4) noisy shrieks. We describe several vocalizations for the first time and provide a clear classification of some of them on the basis of call durations (long/short growls). Complex bark sequences, previously described as distant communication calls, were invariant and were not often emitted by individuals when in close proximity. When classified spectrographically, the remaining 3 call types, which occurred when individuals were in close proximity, were less stereotypical, and gradations within call types were apparent. Our results show that although nocturnal and non-gregarious, complex communicatory signals of bush babies constitute a vocal repertoire formerly thought to be characteristic only of diurnal, gregarious primates.     

Social learning of a communicative signal in captive chimpanzees

The acquisition of linguistic competency from more experienced social partners is a fundamental aspect of human language. However, there is little evidence that non-human primates learn to use their vocalizations from social partners. Captive chimpanzees (Pan troglodytes) produce idiosyncratic vocal signals that are used intentionally to capture the attention of a human experimenter. Interestingly, not all apes produce these sounds, and it is unclear what factors explain this difference. We tested the hypothesis that these attention-getting (AG) sounds are socially learned via transmission between mothers and their offspring. We assessed 158 chimpanzees to determine if they produced AG sounds. A significant association was found between mother and offspring sound production. This association was attributable to individuals who were raised by their biological mother-as opposed to those raised by humans in a nursery environment. These data support the hypothesis that social learning plays a role in the acquisition and use of communicative vocal signals in chimpanzees.     

Individuality of distress and discomfort calls in neonates with bass voices: Wild‐living goitred gazelles (Gazella subgutturosa) and saiga antelopes (Saiga tatarica)

Neonate ruminants produce distress calls when captured by a predator and discomfort milk begging calls when hungry. In many neonate ruminants, the distress and discomfort calls are high‐frequency vocalizations, in which the fundamental frequency is the key variable for recognition of their emotional arousal by caregivers. In contrast, in this study, we examine the low‐frequency open‐mouth distress and discomfort calls in the neonates of two species of wild‐living ungulates, which clearly highlight vocal tract resonances (formants). In the goitred gazelle (Gazella subgutturosa), the distress calls were higher in fundamental frequency (f0) and in the first and third formants than the discomfort calls. The accuracy of classifying individuals by variables of distress calls with discriminant function analysis (67%) was significantly lower than that of discomfort calls (85%). In the saiga (Saiga tatarica), only the third formant was higher in the distress calls than in the discomfort calls. The accuracy of classifying individuals by variables of distress calls (89%) did not differ significantly from that of discomfort calls (94%). Thus, the use of acoustic cues to vocal identity and to the degree of arousal differs between the two species. Calls were significantly more individualistic in the saiga, probably because this species lives in large herds and neonates use a ‘following’ antipredatory strategy, in which vocal individuality is crucial for mother–offspring communication. In contrast, goitred gazelles live in smaller groups and neonates use a ‘hiding’ antipredatory strategy. Accordingly, mothers can rely on additional environmental cues for spotting their young and this may decrease the necessity for individualization of the calls of neonates.     

Structural Classification of Wild Boar (Sus scrofa) Vocalizations

Determining whether a species' vocal communication system is graded or discrete requires definition of its vocal repertoire. In this context, research on domestic pig (Sus scrofa domesticus) vocalizations, for example, has led to significant advances in our understanding of communicative functions. Despite their close relation to domestic pigs, little is known about wild boar (Sus scrofa) vocalizations. The few existing studies, conducted in the 1970s, relied on visual inspections of spectrograms to quantify acoustic parameters and lacked statistical analysis. Here, we use objective signal processing techniques and advanced statistical approaches to classify 616 calls recorded from semi‐free ranging animals. Based on four spectral and temporal acoustic parameters—quartile Q25, duration, spectral flux, and spectral flatness—extracted from a multivariate analysis, we refine and extend the conclusions drawn from previous work and present a statistically validated classification of the wild boar vocal repertoire into four call types: grunts, grunt‐squeals, squeals, and trumpets. While the majority of calls could be sorted into these categories using objective criteria, we also found evidence supporting a graded interpretation of some wild boar vocalizations as acoustically continuous, with the extremes representing discrete call types. The use of objective criteria based on modern techniques and statistics in respect to acoustic continuity advances our understanding of vocal variation. Integrating our findings with recent studies on domestic pig vocal behavior and emotions, we emphasize the importance of grunt‐squeals for acoustic approaches to animal welfare and underline the need of further research investigating the role of domestication on animal vocal communication.     

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.     

Calling at the highway: The spatiotemporal constraint of road noise on Pacific chorus frog communication

Loss of acoustic habitat due to anthropogenic noise is a key environmental stressor for vocal amphibian species, a taxonomic group that is experiencing global population declines. The Pacific chorus frog (Pseudacris regilla) is the most common vocal species of the Pacific Northwest and can occupy human‐dominated habitat types, including agricultural and urban wetlands. This species is exposed to anthropogenic noise, which can interfere with vocalizations during the breeding season. We hypothesized that Pacific chorus frogs would alter the spatial and temporal structure of their breeding vocalizations in response to road noise, a widespread anthropogenic stressor. We compared Pacific chorus frog call structure and ambient road noise levels along a gradient of road noise exposures in the Willamette Valley, Oregon, USA. We used both passive acoustic monitoring and directional recordings to determine source level (i.e., amplitude or volume), dominant frequency (i.e., pitch), call duration, and call rate of individual frogs and to quantify ambient road noise levels. Pacific chorus frogs were unable to change their vocalizations to compensate for road noise. A model of the active space and time (“spatiotemporal communication”) over which a Pacific chorus frog vocalization could be heard revealed that in high‐noise habitats, spatiotemporal communication was drastically reduced for an individual. This may have implications for the reproductive success of this species, which relies on specific call repertoires to portray relative fitness and attract mates. Using the acoustic call parameters defined by this study (frequency, source level, call rate, and call duration), we developed a simplified model of acoustic communication space–time for this species. This model can be used in combination with models that determine the insertion loss for various acoustic barriers to define the impact of anthropogenic noise on the radius of communication in threatened species. Additionally, this model can be applied to other vocal taxonomic groups provided the necessary acoustic parameters are determined, including the frequency parameters and perception thresholds. Reduction in acoustic habitat by anthropogenic noise may emerge as a compounding environmental stressor for an already sensitive taxonomic group.     

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.