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Evolutionary novelties underlie sound production in baleen whales

Nature volume 627, pages 123–129 (2024)Cite this article

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Abstract

Baleen whales (mysticetes) use vocalizations to mediate their complex social and reproductive behaviours in vast, opaque marine environments1. Adapting to an obligate aquatic lifestyle demanded fundamental physiological changes to efficiently produce sound, including laryngeal specializations2,3,4. Whereas toothed whales (odontocetes) evolved a nasal vocal organ5, mysticetes have been thought to use the larynx for sound production1,6,7,8. However, there has been no direct demonstration that the mysticete larynx can phonate, or if it does, how it produces the great diversity of mysticete sounds9. Here we combine experiments on the excised larynx of three mysticete species with detailed anatomy and computational models to show that mysticetes evolved unique laryngeal structures for sound production. These structures allow some of the largest animals that ever lived to efficiently produce frequency-modulated, low-frequency calls. Furthermore, we show that this phonation mechanism is likely to be ancestral to all mysticetes and shares its fundamental physical basis with most terrestrial mammals, including humans10, birds11, and their closest relatives, odontocetes5. However, these laryngeal structures set insurmountable physiological limits to the frequency range and depth of their vocalizations, preventing them from escaping anthropogenic vessel noise12,13 and communicating at great depths14, thereby greatly reducing their active communication range.

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Fig. 1: Adaptations in mysticete laryngeal anatomy.
Fig. 2: A previously undescribed phonation mechanism in mysticetes.
Fig. 3: Computational modelling shows that mysticetes use MEAD principles and unique muscles to control frequency.
Fig. 4: Bilateral TAF phonation in humpback whales.
Fig. 5: The phonation mechanism in two mysticete clades extends the fundamental frequency range of harmonic sounds.

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Data availability

Source data for figures are available at Zenodo (https://doi.org/10.5281/zenodo.10390075). The B. musculus recording is from Discovery of Sounds in the Sea, https://dosits.org/galleries/audio-gallery/marine-mammals/baleen-whales/blue-whale/. The B. mysticus recording is from the Watkins Marine Mammal Sound Database, Woods Hole Oceanographic Institution and the New Bedford Whaling Museum (https://whoicf2.whoi.edu/science/B/whalesounds/index.cfm). Source data are provided with this paper.

Code availability

Code is available at Zenodo (https://doi.org/10.5281/zenodo.10390075).

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Acknowledgements

We thank staff at the Natural History Museum of Denmark, the Fisheries and Maritime Museum and the Danish Nature Agency for their aid in stranding response and dissection of the sei and humpback whales; C. Bie Thøstesen and M. Tange Olsen for help in organizing the dissections; G. Hantke and A. Kitchener for providing the minke whale larynx; C. Herbst and D. Mann for assistance with experiments in Vienna; and L. Jakobsen, P. T. Madsen and D. Wisniewska for comments on the manuscript. Funding was from Carlsberg Foundation CF14-1096 and NovoNordisk grant NFF20OC0063964 to C.P.H.E. and an Austrian Science Fund (FWF) grant W1262-B29 to W.T.F.

Author information

Authors and Affiliations

  1. Sound Communication and Behaviour Group, Department of Biology, University of Southern Denmark, Odense, Denmark

    Coen P. H. Elemans, Mikkel H. Jensen & Magnus Wahlberg

  2. Department of Mechanical Engineering, Rochester Institute of Technology, Rochester, NY, USA

    Weili Jiang, Xudong Zheng & Qian Xue

  3. Department of Behavioral and Cognitive Biology, Faculty of Life Sciences, University of Vienna, Vienna, Austria

    Helena Pichler & W. Tecumseh Fitch

  4. Department of Radiology, Odense University Hospital, Odense, Denmark

    Bo R. Mussman & Jacob Nattestad

  5. Department of Clinical Research, University of Southern Denmark, Odense, Denmark

    Bo R. Mussman

  6. Vienna Cognitive Science Hub, University of Vienna, Vienna, Austria

    W. Tecumseh Fitch

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  1. Coen P. H. Elemans
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Contributions

C.P.H.E., M.H.J. and M.W. carried out experiments on excised larynx in Odense, and C.P.H.E., H.P. and W.T.F. in Vienna. C.P.H.E., B.R.M. and J.N. scanned the preparations and M.H.J. and H.P. annotated the scans. C.P.H.E. designed and built the experimental set-ups in Odense, analysed the experimental data and made figures. W.J., X.Z., C.P.H.E. and Q.X. developed the FSI model. W.J. analysed simulation data and made figures. C.P.H.E. carried out and analysed the material tests. C.P.H.E. and W.T.F. wrote the first drafts of the manuscript, and all authors contributed to the final draft.

Corresponding authors

Correspondence to Coen P. H. Elemans or W. Tecumseh Fitch.

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Extended data figures and tables

Extended Data Fig. 1 Sei whale larynx gross anatomy.

a, 3D render of laryngeal cartilages based on CT scan as in Fig. 1d. b, Ventral view of larynx defrosted after in vitro phonation experiment. Laryngeal sac has been cut medially and the blue tracheal connector is visible. c, Dorsal view of larynx with cricoid cartilage cut and arytenoids bend laterally. d, View on Cricoid Cushion (CC) and Transverse arytenoid folds (TAF) in rest (left) and adducted against each other as during phonation (right). e, Sagittal sections through the CC at various adjacent locations showing the tensor pulvini muscle (deep red) and CC fat (yellow to greenish). Section 7 and 8 have already been frozen in liquid nitrogen. f, 3D render and g, dissection view of medial section through larynx. Indicated are CC sections and TAF sections through the arytenoid cartilage (below).

Extended Data Fig. 2 Humpback whales phonate by CC against TAF vibration.

a, Still of endoscopic view. b, Overview and c, detail of small section of the in vitro sound production data showing that the CC and TAFs vibrate and that sound and acceleration excitation occurs on gap opening.

Extended Data Fig. 3 Tissue motion during phonation on CC and TAF mucosa.

Motion during phonation at Probe 1 and 2 location (Fig. 3f) is larger on CC compared to TAF mucosa (1.84 ± 0.08 vs. 0.32 ± 0.01 mm in Probe 1 location, n = 11 cycles; two-tailed, paired t-test, p = 6.2e−10).

Extended Data Fig. 4 Ingressive flow does not lead to stable self-sustained oscillations of CC against TAF.

a, Laryngeal flow waveform and b, probe readout showing a damped vibration, instead of self-sustained oscillations. See also Supplementary Video 6.

Extended Data Fig. 5 Stimulation of vocalis muscle does not have a notable effect on vocalization frequency.

Three different stimulation levels (α) of the vocalis muscle: a, α = 0; b, α = 0.1; c, α = 0.2. Left, the muscle stress in the fibre direction; Right: Laryngeal flow as a function of time. The fundamental frequency (fo) was obtained by a fast fourier transform of the data from 50 ms to 400 ms.

Extended Data Fig. 6 Strain-stress relationship of the passive component of the modelled muscle tissue.

Left, transverse direction. Right, along the fibre direction.

Extended Data Table 1 Statistical tests
Full size table
Extended Data Table 2 Anatomical and bioacoustic data of mysticete species
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Extended Data Table 3 Material properties in the Sei whale larynx FSI model
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Supplementary information

Supplementary Information

Reporting Summary

Supplementary Audio 1

Aerial sound signal of CC against TAF phonation in sei whale.

Supplementary Audio 2

Acceleration signal of CC against TAF phonation in sei whale.

Supplementary Audio 3

Electroglottograph signal of CC against TAF phonation in sei whale.

Supplementary Audio 4

Aerial sound signal of CC against TAF phonation in minke whale.

Supplementary Audio 5

Electroglottograph signal of CC against TAF phonation in minke whale.

Supplementary Audio 6

Aerial sound signal of CC against TAF phonation in humpback whale.

Supplementary Audio 7

Acceleration signal of CC against TAF phonation in humpback whale.

Supplementary Audio 8

Electroglottograph signal of CC against TAF phonation in humpback whale.

Supplementary Audio 9

Aerial sound signal of bilateral TAF phonation in humpback whale.

Supplementary Audio 10

Acceleration signal of bilateral TAF phonation in humpback whale.

Supplementary Video 1

Supplementary Video 2

Supplementary Video 3

Supplementary Video 4

Supplementary Video 5

Supplementary Video 6

Supplementary Video 7

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Elemans, C.P.H., Jiang, W., Jensen, M.H. et al. Evolutionary novelties underlie sound production in baleen whales. Nature 627, 123–129 (2024). https://doi.org/10.1038/s41586-024-07080-1

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