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.

Keywords: Acoustic allometry; Bioacoustics; Communication; Functional morphology; Sound visualization; Vocal learning; Vocal signals.

Fig. 1

Schematic figure of vocal tract: (1) larynx (yellow), vocal folds (red), trachea (green), esophagus (orange), (2) velum (blue), (3) tongue (pink), (4) nasal cartilages (violet); facial musculature: (a) musculus (m.) temporalis, (b) m. masseter, (c) m. buccinator, (d) m. orbicularis oris. The relative position of the skull is depicted in the background

Fig. 2

Facial movements (f, 55 years) during squeak production and the corresponding narrowband spectrogram: a Mouth relaxed and slightly open in resting position, b mouth closing in preparation of squeak production, c mouth fully closed and labial angles retracted at squeak onset, d,e cheeks depressed successively during squeak production, and f mouth relaxed again. Pictures were extracted from the video Additional file 1, where more subjects can be viewed squeaking

Fig. 3

Spectrogram and acoustic camera images: a Squeak (2nd harmonic) orally emitted (f, 60 years). b Squeak (F0) orally emitted by other individual (f, 55 years). c Snort simultaneously uttered through the trunk

Fig. 4

Anatomical details of mouth and lips: a Asian elephant skull in frontal view and b view into the oral cavity from below the maxilla. c, d Mouth opened on command in c m, 7 years and d f, 35 years. e, f Mouth closing and opening while feeding (f, 45 years), e tongue visible in the middle and upper lips above labial angles and f mouth fully closed, note the two sides of the lower lip slightly overlapping while the tip of the lip hangs loosely, images from Video S2. g Frontal view of closed mouth, trunk lifted during social interaction (f, 42 years)

Fig. 5

Spectrograms: a–d Squeaks from four different adult female Asian elephants demonstrating intra-individual (a + b) and interindividual (a–d) variability in spectral and temporal features and containing examples of nonlinear phenomena: a long squeaks that were emitted as single calls and concatenated for display (f, 55 years), b short squeaks that were emitted in a bout (f, 23 years); c f, 60 years, d f, 48 years, e the first author whistling; f a balloon when letting the air stream through its tensed neck; and g the first author buzzing her lips

Fig. 6

Squeak mean F0 across call (Hz) plotted against age (years). Fitted regression line (y = 895.8–2.670x) for 13 females (black symbols) (N_calls = 225, N_call/subject = 4–30, χ² = 0.419, df = 4, P value = 0.51, Table S4), and 3 males that are not included in the model (red symbols)