Abstract
BackgroundAnatomical 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.ResultsWe 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.ConclusionOur 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.
Highlights
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
Facial movements and respiration during squeak production Squeak onset coincided with a conspicuous movement of oromandibular and orofacial muscles (Fig. 2 and video Additional file 1) that initially suggested their involvement in sound production
We revealed that Asian elephants use a novel mechanism, “lip buzzing,” to produce vocal signals beyond the already extensive frequency range of laryngeal and trunk-based calls
Summary
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 They are among the few evolutionarily distantly related animals (humans, pinnipeds, cetaceans, birds) capable of imitating species-atypical sounds. The instrument merely forms the spectral structure by resonating the sound produced by the vibration of the “buzzing lips.” This principle parallels the sourcefilter theory of vocal production [4, 5], whose application beyond human speech fostered a growing understanding of how morphology and information content covary in animal signals [6]. The elephants’ high-frequency “trumpet” (F0 ~ 300–500 Hz) [17] is assumed to be produced via paired valve-shaped cartilages at the lateral sides of each of the nasal cavities set into vibration by vigorous exhalation of air [18] with no involvement of the larynx [19] (Fig. 1)
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