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.

Elephants and Sirenians: A Comparative Review across Related Taxa in Regard to Learned Vocal Behavior

“…Some individuals have been observed applying nasal tissue vibration via an ingressive airflow at the trunk tip to produce extraordinary high-frequency sounds (reaching a f 0 of up to 1800 Hz; . These examples demonstrate the elephant's ability to use alternative sound production strategies to overcome morpho-mechanical limitations of laryngeal sound production to extend the frequency range available for communication (Beeck et al, 2021;) with a mechanism that potentially combines motoric abilities with vocal learning processes.…”

“…Usage and functionality may differ, however, as African elephants appear to trumpet and Asian elephants tend to roar more often in situations of arousal (Stoeger & de Silva, 2014). Another high-pitched call type is the squeak (f 0 mean = 813.07 Hz), which is produced by Asian elephants via lip buzzing (Beeck et al, 2021;Stoeger & de Silva, 2014) in alarming or socially arousing contexts (de Silva, 2010; Herler & Stoeger, 2012;Nair et al, 2009). Squeaks have been heard from a few African savannah elephants; however, these are either imitations (of Asian elephant squeaks) or sound creations, respectively .…”

“…Although the mode of rumble production is understood, the mechanism and anatomical sound-producing structures behind the higher-frequency vocalizations remain speculative, because the elephant's massive vocal folds can most likely not generate these high frequencies. A recent study suggested that Asian elephants produce their species-specific high-pitched squeaks (with a f 0 of up to 2000 Hz) by self-sustained lip vibrations when forcing air through tensed lips (also termed lip buzzing; Beeck et al, 2021). In addition, African savanna elephants produce a variety of idiosyncratic sounds (Poole, 2011;Stoeger & Manger, 2014).…”

“…Besides the larynx, walruses use their pharyngeal pouches, teeth, nose and mouth, the lips, and the mobile tongue to produce sounds (Schusterman & Reichmuth, 2008). Elephants also make use of their lips (Beeck et al, 2021), tongue, and the multifunctional trunk to modify and to generate sounds. Manatees possess a highly flexible mouth with prehensile lips; the upper lip pad is split into left and right sides, which can move independently (Noll, 1983).…”

Author Correction to: A novel theory of Asian elephant high-frequency squeak production

“…Following publication of the original article [ 1 ], the authors noticed that an incorrect file for Additional file 4 was captured. The corrected version of Additional file 4 is attached to this Correction and Additional file 4 has been updated in the original article accordingly.…”