Monkeys Yodel Better Than Us? Vocal Membranes Behind Wild Pitch Shifts

In a recent study published in Philosophical Transactions B, researchers investigated transitions in fundamental frequency (fo) vocalizations of New World monkeys.

Understanding fo transitions in primate vocalization could provide valuable insights into the evolutionary aspects of their vocal communication and guide animal care practices.

Red-faced spider monkey, Ateles paniscus hanging in some ropes.​​​​​​​Study: ‘Monkey yodels’—frequency jumps in New World monkey vocalizations greatly surpass human vocal register transitions. Image Credit: MJphotographics/Shutterstock.com

Introduction

Fundamental frequency jumps are abrupt transitions between distinct oscillatory states of the laryngeal voice source. These transitions occur in the vocalization of several non-human primates (NHPs) and are similar to human yodeling. There are two primary human vocal registers: M1 (modal, low fo) for speech and M2 (falsetto, high fo) for singing.

Primates like New World monkeys exhibit laryngeal mechanisms similar to human registers. Notably, their larynx has an additional oscillating structure, the vocal membranes, that extend upwards from the vocal folds.

These membranes may enable distinct laryngeal vibrations analogous to voice registers in humans. However, there is limited research on vocal registers in animal bioacoustics. Knowledge of the mechanisms underlying laryngeal vibrations is sparse.

About the Study

In the present study, researchers investigated the role of laryngeal vocal membranes in the voice production mechanisms of NHPs using New World monkeys as models.

The researchers explored vocalization mechanisms in 12 monkeys representing six species (Alouatta sara, Alouatta caraya, Ateles chamek, Saimiri boliviensis, Sap. Apella, and Cebus albifrons). They recorded vocalizations while staff gently held the animals.

They monitored electroglottograph (EGG) signals alongside acoustic signals at a sampling frequency of 48 kHz to assess laryngeal production. EGG signals were captured using electrodes placed on the larynx and digitized for analysis.

To acquire ex vivo data, the team studied larynges of tufted capuchin monkeys excised post-euthanasia for research purposes. They scanned the specimens by diffusible iodine-based contrast-enhanced computed tomography (diceCT) to compare the anatomical configurations of larynges across species. They also assessed changes in laryngeal voice production based on arytenoid position.

Humidified air generated oscillations in laryngeal tissue during experiments. Subglottal pressure was varied to assess its effects on vocal fold oscillation. High-speed video recorded vocal fold vibrations for analysis.

The team analyzed 1,375 vocalization samples, of which 64 were high-quality. They annotated low-fo and high-fo portions in the vocalizations. They used the Neubauer mathematical model to simulate vocal dynamics.

Researchers analyzed kymograms that plotted mediolateral deflections of the laryngeal truss against time. To simulate the register-like transitions in humans, they switched between alternate modes of oscillations involving the vocal fold with and without vocal membranes.

Results

The team observed two modes of vocal vibrations in three species. The first involved only the vocal folds to produce low-frequency oscillations (low fo) analogous to those underlying human phonetic sounds.

The second incorporated the vocal membranes in addition to vocal folds to generate high-frequency oscillations (high fo). The transition between these two mechanisms occurs within a few glottal cycles and thus indicates a bifurcation phenomenon.

The dual mechanism that generates low fo and high fo oscillations provides a deeper insight into how monkeys control their vocal output, contrasting with simplified vocal production mechanisms in humans.

The loss of certain anatomical features in humans may have led to a more stable but less complex vocal production system, highlighting the evolutionary trade-offs in vocal communication.

The excised laryngeal experiments showed considerable shifts in oscillatory mechanisms after arytenoid cartilage manipulation, indicating that vocal membranes play a crucial role in fo transitions. Medial and lateral rotations of the arytenoid generated high and low fo oscillations, respectively.

The team observed abrupt jumps in fundamental frequency in the obtained datasets. While these jumps are akin to rapid frequency transitions in certain styles of human singing (e.g., yodeling), they are much larger in primates.

Fundamental frequency jumps in New World monkeys reached ratios of up to 12, while human transitions generally range from 1.2 to 2.5. The findings suggest that these primates use unique anatomical features, particularly pronounced vocal membranes, to achieve complex vocal expressions.

Conclusions

Based on the findings, abrupt fo jumps occurring during New World monkey vocalizations drive distinct laryngeal vibrations. These jumps surpass human vocal register transitions, indicating that non-human primates such as New World monkeys use unique anatomical features to generate vocal sounds. Among the monkeys, the fo transitions involve low fo and high fo states.

While vocal folds generate low fo vibrations, vocal membranes produce high fo vibrations. Thus, vocal membranes are crucial in shaping laryngeal vocalizations among NHPs.

While the low fo and high fo states among primates are similar to human vocal registers, the vocal membranes, absent in humans, provide unique vocal abilities to primates. The study suggests that distinct laryngeal mechanisms may produce distinct call types in animals.

Future studies could investigate these laryngeal mechanisms to guide care practices based on vocal communication in social contexts, such as attention-grabbing, signaling, or avoiding habituation among groups.

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