The multi-dimensional nature of vocal learning

Funding; S.C.V. was supported by a Max Planck Research Group (MPRG), a Human Frontiers Science Program (HFSP) Research grant (grant no. RGP0058/2016) and a UKRI Future Leaders Fellowship (grant no. MR/T021985/1). P.L.T. was supported by US Office of Naval Research (ONR) grant nos N00014-18-1-2062 and N00014-20-1-2709. B.P.K. was supported by the European Union's Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement no. 751356. V.C.B. was supported by the DK Cognition and Communication by the Austrian Science Fund (FWF) grant no. W1262-B29.How learning affects vocalizations is a key question in the study of animal communication and human language. Parallel efforts in birds and humans have taught us much about how vocal learning works on a behavioural and neurobiological level. Subsequent efforts have revealed a variety of cases among mammals in which experience also has a major influence on vocal repertoires. Janik and Slater (Anim. Behav.60, 1–11. (doi:10.1006/anbe.2000.1410)) introduced the distinction between vocal usage and production learning, providing a general framework to categorize how different types of learning influence vocalizations. This idea was built on by Petkov and Jarvis (Front. Evol. Neurosci.4, 12. (doi:10.3389/fnevo.2012.00012)) to emphasize a more continuous distribution between limited and more complex vocal production learners. Yet, with more studies providing empirical data, the limits of the initial frameworks become apparent. We build on these frameworks to refine the categorization of vocal learning in light of advances made since their publication and widespread agreement that vocal learning is not a binary trait. We propose a novel classification system, based on the definitions by Janik and Slater, that deconstructs vocal learning into key dimensions to aid in understanding the mechanisms involved in this complex behaviour. We consider how vocalizations can change without learning, and a usage learning framework that considers context specificity and timing. We identify dimensions of vocal production learning, including the copying of auditory models (convergence/divergence on model sounds, accuracy of copying), the degree of change (type and breadth of learning) and timing (when learning takes place, the length of time it takes and how long it is retained). We consider grey areas of classification and current mechanistic understanding of these behaviours. Our framework identifies research needs and will help to inform neurobiological and evolutionary studies endeavouring to uncover the multi-dimensional nature of vocal learning.Publisher PDFPeer reviewe

Sound production of Asian elephant high-frequency vocalisations

Anatomical and cognitive adaptations to overcome morph-mechanical constraints of the vocal folds increase vocal diversity across taxa. The Asian elephants´ vocal repertoire ranges from infrasonic rumbles (F0 ~ 20 Hz) to higher pitched trumpets (F0 340-540 Hz) and species-specific squeaks (F0 300-2300 Hz). While rumbles are congruent with vocal fold vibration in large sized mammals, trumpets and squeaks were hypothesised to be emitted by the trunk without current knowledge of the sound source. We use an acoustic camera to visualise nasal trumpet but oral squeak emission and an event of simultaneous oral and nasal emission (biphonation) in a captive group of female Asian elephants. By combining these findings with acoustic, behavioural and morphological data we suggest that trumpets are produced by vibration of nasal cartilages, but squeaks by vibration of the tensely closed lips. Our data further suggests that context or vocal production learning might be involved in squeak sound productio

Sound production of Asian elephant high-frequency vocalisations

Anatomical and cognitive adaptations to overcome morph-mechanical constraints of the vocal folds increase vocal diversity across taxa. The Asian elephants´ vocal repertoire ranges from infrasonic rumbles (F0 ~ 20 Hz) to higher pitched trumpets (F0 340-540 Hz) and species-specific squeaks (F0 300-2300 Hz). While rumbles are congruent with vocal fold vibration in large sized mammals, trumpets and squeaks were hypothesised to be emitted by the trunk without current knowledge of the sound source. We use an acoustic camera to visualise nasal trumpet but oral squeak emission and an event of simultaneous oral and nasal emission (biphonation) in a captive group of female Asian elephants. By combining these findings with acoustic, behavioural and morphological data we suggest that trumpets are produced by vibration of nasal cartilages, but squeaks by vibration of the tensely closed lips. Our data further suggests that context or vocal production learning might be involved in squeak sound productio

A novel theory of Asian elephant high-frequency squeak production

Abstract Background Anatomical and cognitive adaptations to overcome morpho-mechanical limitations of laryngeal sound production, where body size and the related vocal apparatus dimensions determine the fundamental frequency, increase vocal diversity across taxa. Elephants flexibly use laryngeal and trunk-based vocalizations to form a repertoire ranging from infrasonic rumbles to higher-pitched trumpets. Moreover, they are among the few evolutionarily distantly related animals (humans, pinnipeds, cetaceans, birds) capable of imitating species-atypical sounds. Yet, their vocal plasticity has so far not been related to functions within their natural communicative system, in part because not all call types have been systematically studied. Here, we reveal how Asian elephants (Elephas maximus) produce species-specific squeaks (F0 300–2300 Hz) by using acoustic camera recordings to visualize sound emission and examining this alongside acoustic, behavioral, and morphological data across seven captive groups. Results We found that squeaks were emitted through the closed mouth in synchrony with cheek depression and retraction of the labial angles. The simultaneous emission of squeaks with nasal snorts (biphonation) in one individual confirmed that squeak production was independent of nasal passage involvement and this implicated oral sound production. The squeaks’ spectral structure is incongruent with laryngeal sound production and aerodynamic whistles, pointing to tissue vibration as the sound source. Anatomical considerations suggest that the longitudinal closed lips function as the vibrators. Acoustic and temporal parameters exhibit high intra- and inter-individual variability that enables individual but no call-subtype classification. Only 19 of 56 study subjects were recorded to squeak, mostly during alarming contexts and social arousal but some also on command. Conclusion Our results strongly suggest that Asian elephants force air from the small oral cavity through the tensed lips, inducing self-sustained lip vibration. Besides human brass players, lip buzzing is not described elsewhere in the animal kingdom. Given the complexity of the proposed mechanism, the surprising absence of squeaking in most of the unrelated subjects and the indication for volitional control, we hypothesize that squeak production involves social learning. Our study offers new insights into how vocal and cognitive flexibility enables mammals to overcome size-related limitations of laryngeal sound production. This flexibility enables Asian elephants to exploit a frequency range spanning seven octaves within their communicative system