Carlson, D.

de Reus, K.

Garcia, M.

Gross, S.

Lowry, A.

Ravignani, A.

Rubio-García, A.

Salazar-Casals, A.

English

MPG.PuRe

   BODY SIZE PREDICTS VOCAL TRACT SIZE IN A MAMMALIAN VOCAL LEARNER KOEN DE REUS*1,2,3, DARYLL CARLSON3,4, ALICE LOWRY3,5, STEPHANIE GROSS6, MAXIME GARCIA7,8, ANA RUBIO-GARCIA3, ANNA SALAZAR-CASALS3, and ANDREA RAVIGNANI1,3,9 *Corresponding Author: koen.dereus@mpi.nl 1Comparative Bioacoustics Group, Max Planck Institute for Psycholinguistics, Nijmegen, Netherlands 2Artificial Intelligence Lab, Vrije Universiteit Brussel, Brussels, Belgium 3Research Department, Sealcentre Pieterburen, Pieterburen, Netherlands 4Department of Earth System Science, Stanford University, Stanford, USA 5School of Environmental Science, University of Liverpool, Liverpool, UK 6Institute for Terrestrial and Aquatic Wildlife Research (ITAW), University of Veterinary Medicine Hannover, Foundation, Büsum, Germany 7Animal Behaviour, Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zürich, Switzerland 8Center for the Interdisciplinary Study of Language Evolution, University of Zurich, Zürich, Switzerland 9Center for Music in the Brain, Department of Clinical Medicine, Aarhus University & The Royal Academy of Music Aarhus/Aalborg, Aarhus, Denmark  1. Mechanisms for escaping acoustic allometry Animals whose call features do not scale with their body size are said to escape acoustic allometry. These animals may thus sound smaller or larger than they are. Recent work (Garcia & Ravignani, 2020; Ravignani & Garcia 2021) found that they can achieve this by evolving vocal tract modifications (e.g., laryngeal descent; Reby & McComb, 2003) or by learning to better control their vocal organs (i.e., vocal learning, Janik & Slater, 1997). To identify which mechanism is used by species to escape acoustic allometry, one could perform an anatomical study to test if vocal tract size scales with body size. Acoustic allometry is escaped by anatomical adaptations if vocal tract size does not scale with body size, and through vocal learning if there is scaling between vocal tract size and body size.  154This paper is distributed under a Creative Commons BY-NC-ND 3.0 license.    2. Anatomical studies can help find more vocal learners Studies that test whether animal vocal tracts scale with their body size offer a simple way of testing the hypothesis pitting anatomical adaptations vs. vocal learning (Garcia & Ravignani, 2020; Ravignani & Garcia 2021). Moreover, they can help to identify new species capable of vocal learning, a prerequisite for human speech. Adopting a comparative approach which considers an increasing number of vocal learning species could offer promising insights into the biological underpinnings of communication systems such as spoken language.  3. Harbor seal vocal tracts scale with their body size Harbor seals’ (Phoca vitulina) large vocal plasticity allows them to modulate the call frequencies they produce (Ralls et al., 1985; Torres Borda et al., 2021), enabling them to produce sounds with different frequencies than predicted from their body size. The current study tests if the vocal tract of the harbor seal, a known mammalian vocal learner, scales with its body size (de Reus et al., 2022). Vocal tracts, including larynges, of 68 young harbor seals (pups and weaners) were measured using a caliper and tested for allometry with body size using generalized linear mixed models. We find that both body length and body mass predict vocal tract length, vocal fold length, and tracheal dimensions (Table 1). Interestingly, allometry between body size and vocal fold length emerges after puppyhood, suggesting that ontogeny may modulate the anatomy vs. learning distinction. We conclude that the vocal tracts of harbor seals do indeed scale with body size. Consequently, by exclusion, vocal learning is the likely mechanism used in young harbor seals to escape acoustic allometry.  Table 1. Selected models for each vocal tract measurement.  Measurement Model Deviance explained Vocal tract length BL+BM+A+S+BL*S 59.30% Vocal fold length BL+BM+A+S+A*BM+A*S 74.89% Subglottic-tracheal dorsoventral distance 1 BL+BM+A+S 69.99% Subglottic-tracheal dorsoventral distance 2 BL+BM+A+S 58.38% Note. BL = body length, BM = body mass, A = age class, S = sex. Predictor terms joined by an asterisk denote an interaction. Significant predictor terms are underlined.  155   Acknowledgements We would like to thank all members of Sealcentre Pieterburen for their continued support in this research. In particular, we are grateful to Letty Stupers, Rebecca Andreini, and Maria Jose Robles for help in data collection. We thank Aline Joustra for her illustrations of harbor seal vocal tracts. We also greatly appreciate the extensive comments provided by Taylor Hersh, Laura Verga, Yannick Jadoul, and Limor Raviv. This work was supported by a Max-Planck-Gesellschaft (Max Planck Research Group, MPRG) and a Fonds Wetenschappelijk Onderzoek (FWO) Pegasus Marie Curie fellowship 12N5517N awarded to A.R. K.d.R. was supported by the Fonds Wetenschappelijk Onderzoek project ‘Interactive vocal rhythms’ G034720N awarded to Bart de Boer. The German Ministry of Energy, Agriculture, the Environment, Nature and Digitalization (MELUND) funded the marine mammal stranding scheme and the necropsies in Schleswig-Holstein. The Sealcentre Pieterburen funded the seal stranding scheme and the necropsies at the Sealcentre Pieterburen. M.G. was supported by a research grant from the Ethologische Gesellschaft e.V., as well as a postdoctoral research grant from the Forschungskredit of the University of Zurich [grant no. FK-21-121].   References de Reus, K., Carlson, D., Lowry, A., Gross, S., Garcia, M., Rubio-Garcia, A., ... & Ravignani, A. (2022). Vocal tract allometry in a mammalian vocal learner. Journal of Experimental Biology, 225(8), jeb243766. Garcia, M., & Ravignani, A. (2020). Acoustic allometry and vocal learning in mammals. Biology Letters, 16(7), 20200081. Janik, V. M., & Slater, P. J. (1997). Vocal learning in mammals. In: P. Slater, C. Snowdon, J. Rosenblatt, & M. Milinski (Eds.), Advances in the Study of Behaviour, 26, 59-100. Ralls, K., Fiorelli, P., & Gish, S. (1985). Vocalizations and vocal mimicry in captive harbor seals, Phoca vitulina. Canadian Journal of Zoology, 63(5), 1050–1056. Ravignani, A., & Garcia, M. (2021). A cross-species framework to identify vocal learning abilities in mammals. Philosophical Transactions of the Royal Society B, 377(1841), 20200394. Reby, D., & McComb, K. (2003). Anatomical constraints generate honesty: Acoustic cues to age and weight in the roars of red deer stags. Animal Behaviour, 65(3), 519–530. Torres Borda, L., Jadoul, Y., Rasilo, H., Casals, A. S., & Ravignani, A. (2021). Vocal plasticity in harbour seal pups. Philosophical Transactions of the Royal Society B: Biological Sciences. 376, 20200456. 156

Body size predicts vocal tract size in a mammalian vocal learner

http://hdl.handle.net/21.11116/0000-000A-FDAB-9

Body size predicts vocal tract size in a mammalian vocal learner

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