Uncovering the voice of toothed whales: A distinct nasal structure helps produce diverse sounds

AMERICAN ASSOCIATION FOR THE ADVANCEMENT OF SCIENCE (AAAS)

Toothed whales like dolphins, orcas, and sperm whales produce their diverse repertoire of sounds through a distinct structure in the nasal passages, but in a way that is strikingly similar to the way terrestrial animals use the larynx or syrinx for vocalization. In a new study, researchers who employed four different techniques to get to the bottom of how these animals make the sounds they do describe this novel sound production system and show how it enables toothed whales to use different vocal registers for echolocation and communication. To date, vocal registers have been confirmed only in humans and crows. Odontocetes (toothed whales) navigate and hunt prey in deep, dark marine environments using echolocation, a strategy that relies on the producing short, rapid and powerful ultrasonic echolocation clicks, which for some species can approach a blistering 200 decibels in volume – just shy of the loudest sounds ever recorded. In addition, toothed whales can produce an acoustically rich collection of grunts, bursts, and whistles used to compose complex vocalizations used for social communication. While its thought that these sounds are created through an airflow-driven sound source called the phonic lips located in the nose, the mechanisms that enable such complex sound production, particularly at depths hundreds of meters below the surface, remain largely unknown. Using a combination of interdisciplinary methods that past studies have lacked – including in vivo imaging and recording in trained whales, novel in vitro laboratory experiments, and techniques used to study sound variation in the human voice – Peter Madsen and colleagues show that odontocete sounds are produced through the nasal passages in a way that is functionally analogous to laryngeal and syringeal sound production in other terrestrial vertebrates, like humans and birds. According to the authors, where laryngeal sound would be hampered by pressure and minimal respiratory air volume, passing air through the nasal passage allows complex sounds to be generated at depths these animals frequent. Madsen et al. also discovered that toothed whales use different vocal registers, namely vocal fry, chest, and falsetto voice, to generate the fundamentally different tones used for echolocation and vocal communication. In a related Perspective, Andrea Ravignani and Christian Herbst discuss the study in greater detail.

**This paper is related to an Annual Meeting Briefing for Science, titled “Uncovering the voice of toothed whales: a distinct nasal structure helps produce diverse sounds,” to be held on March 2nd at 9:00 am US ET. You can access the briefing virtually here if you are registered for the AAAS Annual Meeting. (Please add briefing link to your calendars).

NOTE: If you’d like to attend this and other briefings at the 2023 Annual Meeting and have not yet registered, please do so by March 1st [Register Here. At the Registration Access Code step, please enter PRESS.]**

JOURNAL

Science

DOI

10.1126/science.adc9570

ARTICLE TITLE

Toothed whales use distinct vocal registers for echolocation and communication

ARTICLE PUBLICATION DATE

3-Mar-2023

Toothed whales catch food in the deep using vocal fry

Peer-Reviewed Publication

UNIVERSITY OF SOUTHERN DENMARK

Sperm whale tagging mp4 — VIDEO: CAPTION: DEPLOYMENT OF A SOUND RECORDING TAG ON THE SOUND PRODUCING NOSE OF A SPERM WHALE. CREDIT LINE: PER G. HENRIKSEN, AARHUS UNIVERSITY view more
CREDIT: PER G. HENRIKSEN, AARHUS UNIVERSITY, DENMARK.

Dolphins and other toothed whales are large brained top predators that captivate our imagination; they are extremely social, they cooperate, and can hunt prey down to 2 km deep in complete darkness with echolocation.

All these remarkable behaviors are mediated using sound that travels far and fast in murky and dark waters. However, it has remained a mystery how these amazing animals make their rich vocal repertoires in the deep.

Now a new study in the prestigious journal Science reports that toothed whales evolved an air-driven nasal sound source that operates at different vocal registers like the human voice.

The study was led by Professor Coen Elemans, voice scientist at the Department of Biology, University of Southern Denmark and Professor Peter Madsen, whale biologist at the Department of Biology, Aarhus University in Denmark.

The study shows that toothed whales, like humans, have at least three voice registers; the vocal fry register (also known as creaky voice, which produces the lowest tones), the chest register (which is our normal speaking voice) and the falsetto register (which produces even higher frequencies).

“Vocal fry is a normal voice register that is often used in American English. Kim Kardashian, Kate Perry and Scarlet Johannsen are well-known people using this register”, Professor Elemans says.

According to the new research, toothed whales use this vocal fry register to produce their echolocation calls to catch prey.

“During vocal fry, the vocal folds are only open for a very short time, and therefore it takes very little breathing air to use this register”, Elemans adds.

“And this air-economy makes it especially ideal for echolocation”, says Professor Madsen, adding:

“During deep dives, all air is compressed to a tiny fraction of the volume on the surface”.

Toothed whales dive as deep as 2.000 meters and catch more fish than the human fishing industry. When they hunt in the deep and murky waters, they produce short, powerful, ultrasonic echolocation clicks at rates up to 700 per second to locate, track and catch prey.

“Thus vocal fry allows whales access to the richest food niches on earth; the deep ocean”, says Madsen.

“While vocal fry may be controversial in humans and may be perceived as everything from annoying to authoritative, it doubtlessly made toothed whales an evolutionary success story”, Elemans adds.

It was previously thought that toothed whales make sounds with their larynx just as other mammals, but 40 years ago it became clear that this is not the case; they somehow use their nose to produce sound. In the new study, the Danish research team has uncovered, what exactly goes on using high-speed video through endoscopes:

The toothed whales have evolved an air-driven sound production system in their nose, that functions physically analogous to laryngeal and syringeal sound production in mammals and birds – but its location is far from the same.

“Evolution has moved it from the trachea into the nose, which allowed much higher driving pressures – up to 5 times what a trumpet player can generate - without damaging lung tissues”, says Madsen.

“This high driving pressure allows toothed whales to make the loudest sounds of any animal on the planet,” Elemans adds.

At depths over 100m, whale lungs collapse to avoid compression sickness and are thus no good for air supply, and the remaining air is found in the nasal passages of the skull. This provides a small, but sufficient airspace to produce echolocating sound at astonishing depths of 2000 meters.

When echolocating, toothed whales pressurize air in their bony nose and lets it pass structures called phonic lips that vibrate just as human vocal folds. Their acceleration produces sound waves that travel through the skull to the front of the head.

In addition to echolocation, toothed whales make a huge array of sounds for their complex social communication.

“Some species, like killer and pilot whales, make very complex calls that are learned and passed on culturally like human dialects”, says Madsen.

In their study the researcher show that these sounds are made by the phonic lips vibrating in the chest and falsetto registers. They filmed the phonic lips using several different approaches, using both trained dolphins and animals in the wild that were moving freely with a small tag that recorded their sounds. The in vivo recordings were done at Dolfinarium Harderwijk in Holland.

“It took us close to 10 years to develop new techniques, gather and analyze all our data”, says Elemans.

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