Where does the air go? Anatomy and functions of the respiratory tract in the humpback whale (Megaptera novaeangliae)

Authors

  • Joy S. Reidenberg Icahn School of Medicine at Mount Sinai New York City, NY

Keywords:

humpback whale, larynx, anatomy, respiratory system, vocal tract, sound production

Abstract

Air is a limited resource under water. Pressure changes during diving and ascent further affect buoyancy and sound production/transmission by changing air volumes, densities, and shapes of air spaces and vibration pathways. This paper will focus on how humpback whales use air, and the respiratory tract adaptations that help overcome these challenges. These highly modified respiratory tract tissues function to shunt air to increase oxygenation for extending breath-hold time, conserve and recycle air, maintain hearing at depth, generate sound for communication and navigation, transmit vibrations to water, mitigate noise, support air spaces from collapsing, regulate chamber volumes, produce bubbles as visual signals, control air release as a tool to trap prey, modify center of gravity, regulate buoyancy, and reduce energy expenditure during locomotion. The humpback whale is able to utilize air in an aquatic environment in ways that allow it to support a wide range of unique behaviors.

 

Résumé

L’air est une ressource limitée sous l'eau. Les changements de pression au cours de la plongée et de la remontée affectent la flottabilité et la production / transmission des sons en changeant les volumes d'air, les densités et les formes des espaces aériens et des voies de vibration. Cet article se penche sur la façon dont les baleines à bosse utilisent l'air ainsi que les adaptations des voies respiratoires qui participent au processus. Les tissus des voies respiratoires sont hautement modifiés et fonctionnent de manière à shunter l’air pour augmenter l'oxygénation afin de prolonger le temps d'apnée, de conserver et de recycler l'air, de maintenir l'audition en profondeur, de générer des sons pour la communication et la navigation, de transmettre des vibrations à l'eau, d'atténuer le bruit, d’empêcher les espaces devant contenir l'air de s'effondrer, de réguler les volumes des chambres, de produire des bulles servant de signaux visuels, de réguler la libération de l'air qui servira d’outil pour piéger des proies, de modifier le centre de gravité, de réguler la flottabilité, et enfin de réduire les dépenses d'énergie lors de la locomotion. La baleine à bosse utilise l'air dans un milieu aquatique de manière à assurer une multitude de comportements uniques.

Author Biography

Joy S. Reidenberg, Icahn School of Medicine at Mount Sinai New York City, NY

Professor, Center for Anatomy and Functional Morphology

References

Adam, O., Cazau, D., Gandilhon, N., Fabre, B., Laitman, J. T. and Reidenberg, J. S. 2013. New acoustic model for humpback whale sound production. Applied Acoustics 74, 10: 1182–1190. <https://doi.org/10.1016/j.apacoust.2013.04.007>

Au, W., James, D. and Andrews, K. 2001. High frequency harmonics and source level of humpback whale songs. The Journal of the Acoustical Society of America 110, 5: 2770. <https://doi.org/10.1121/1.4777702>

Au, W. W. L., Pack, A. A., Lammers, M. O., Herman, L. M., Deakos, M. H. and Andrews, K. 2006. Acoustic properties of humpback whale songs. The Journal of the Acoustical Society of America 120, 2: 1103–1110. <https://doi.org/10.1121/1.2211547>

Buono, M. R., Reidenberg, J. S. and Fernández, M. S. 2015. Anatomy of the nasal complex in the southern right whale, Eubalaena australis (Cetacea, Mysticeti). Journal of anatomy 226, 1: 81–92. <https://doi.org/10.1111/joa.12250>

Cazau, D., Adam, O., Laitman, J. T. and Reidenberg, J. S. 2013. Understanding the intentional acoustic behavior of humpback whales: A production-based approach. The Journal of the Acoustical Society of America 134, 3: 2268–2273. <https://doi.org/10.1121/1.4816403>

Clapham, P. 2017. Humpback whale Megaptera novaeangliae. In: Encyclopedia of Marine Mammals. B. Würsig, J. G. M. Thewissen and K. M. Kovacs (eds.), pp 489–492. Academic press, Cambridge, MA.

Cranford, T. W. and Krysl, P. 2015. Fin whale sound reception mechanisms: Skull vibration enables low-frequency hearing. PLoS ONE 10, 3: e0122298. <https://doi.org/10.1371/journal.pone.0116222>

Cranford, T. W., Krysl, P. and Amundin, M. 2010. A new acoustic portal into the odontocetes ear and vibrational analysis of the tympanoperiotic complex. PLoS ONE 5, 8: e11927. <https://doi.org/10.1371/journal.pone.0011927>

Gandilhon, N., Adam, O., Cazau, D., Laitman, J. T. and Reidenberg, J. S. 2015. Two new theoretical roles of the laryngeal sac of humpback whales. Marine Mammal Science 31, 2: 774–781. <https://doi.org/10.1111/mms.12187>

Herman, L. M., Pack, A. A., Spitz, S. S., Herman, E. Y. K., Rose, K., et al. 2013. Humpback whale song: who sings? Behavioral Ecology and Sociobiology 67, 10: 1653–1663. <https://doi.org/10.1007/s00265-013-1576-8>

Ketten, D. R. 2000. Cetacean ears. In: Hearing by Whales and Dolphins. W. L. Au, A. N. Popper and R. R. Fay (eds.), pp 43–108. Springer, New York.

Koopman, H. N., Budge, S. M., Ketten, D. R., and Iverson, S. J. 2006. Topographical distribution of lipids inside the mandibular fat bodies of odontocetes: remarkable complexity and consistency. IEEE Journal of Oceanic Engineering 31, 1: 95–106. <https://doi.org/10.1109/JOE.2006.872205>

Kooyman, G. L. and Ponganis, P. J. 1998. The physiological basis of diving to depth: Birds and mammals. Annual Review of Physiology 60, 1: 19–32. <https://doi.org/10.1146/annurev.physiol.60.1.19>

Laitman, J. T. and Reidenberg, J. S. 1999. Evolution of the vocal folds in cetaceans. In: European Research on Cetaceans 12, Proceedings of the Twelfth Annual Conference of the European Cetacean Society, Monaco, 20–24 January 1998. P. G. H. Evans and E. C. M. Parsons (eds.), pp 286–289. European Cetacean Society.

Mercado III, E., Herman, L. M. and Pack, A. A. 2003. Stereotypical sound patterns in humpback whale songs: Usage and function. Aquatic Mammals 29, 1: 37–52.

Mercado III, E., Schneider, J. N., Pack, A. A. and Herman, L. M. 2010. Sound production by singing humpback whales. The Journal of the Acoustical Society of America 127, 4: 2678–2691. <https://doi.org/10.1121/1.3309453>

Reidenberg, J. S. 2007. Anatomical adaptations of aquatic mammals. The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology 290, 6: 507–513. <https://doi.org/10.1002/ar.20541>

Reidenberg, J. S. and Laitman, J. T. 1987. Position of the larynx in Odontoceti (toothed whales). The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology 218, 1: 98–106. <https://doi.org/10.1002/ar.1092180115>

Reidenberg, J. S. and Laitman, J. T. 1988. Existence of vocal folds in the larynx of Odontoceti (toothed whales). The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology 221, 4: 884–891. <https://doi.org/10.1002/ar.1092210413>

Reidenberg, J. S. and Laitman, J. T. 1999. Identifying the sound source in mysticetes. In: European Research on Cetaceans 12, Proceedings of the Twelfth Annual Conference of the European Cetacean Society, Monaco, 20–24 January 1998. P. G. H. Evans and E. C. M. Parsons (eds.), pp 259–261. European Cetacean Society.

Reidenberg, J. S. and Laitman, J. T. 2007a. Blowing bubbles: An aquatic adaptation that risks protection of the respiratory tract in humpback whales (Megaptera novaeangliae). The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology 290, 6: 569–580. <https://doi.org/10.1002/ar.20537>

Reidenberg, J. S. and Laitman, J. T. 2007b. Discovery of a low frequency sound source in mysticeti (baleen whales): Anatomical establishment of a vocal fold homolog. The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology 290, 6: 745–760. <https://doi.org/10.1002/ar.20544>

Reidenberg, J. S. and Laitman, J. T. 2008. Sisters of the sinuses: Cetacean air sacs. The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology 291, 11: 1389–1396. <https://doi.org/10.1002/ar.20792>

Reidenberg, J. S. and Laitman, J. T. 2010. Generation of sound in marine mammals. In: Handbook of Mammalian Vocalization – An Integrative Neuroscience Approach. S. M. Brudzynski (ed.), pp 451–465. Academic Press, London.

Schoenfuss, H. L., Bragulla, H. H., Schumacher, J., Henk, W. G., Craig George, J. and Hillmann, D. J. 2014. The anatomy of the larynx of the bowhead whale, Balaena mysticetus, and its sound-producing functions. The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology 297, 7: 1316–1330. <https://doi.org/10.1002/ar.22907>

Sharpe, F. A. and Dill, L. M. 1997. The behavior of Pacific herring schools in response to artificial humpback whale bubbles. Canadian Journal of Zoology 75, 5: 725–730. <https://doi.org/10.1139/z97-093>

Withers, P. C., Cooper, C. E., Maloney, S. K., Bozlnovic, F. and Cruz Neto, A. P. 2016. Ecological and Environmental Physiology of Mammals. Oxford University Press, Oxford.

Yamato, M., Ketten, D. R., Arruda, J., Cramer, S. and Moore, K. 2012. The auditory anatomy of the minke whale (Balaenoptera acutorostrata): a potential fatty sound reception pathway in a baleen whale. The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology 295, 6: 991–998. <https://doi.org/10.1002/ar.22459>

Schematic diagram of a Humpback whale head. Joy S Reidenberg. Madagascar Conservation & Development. Megaptera novaeangliae

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Published

19-12-2018

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