Low Frequency Sound Production and Reception in Mammals

Low frequency sounds have longer wavelengths than high frequencies. Because wavelength is equal to the speed of sound divided by frequency, the wavelength for any given frequency is approximately 4.5 times longer in water than in air. Lower frequencies can propagate farther with less transmission loss than higher frequencies in both air and water. Consequently, low frequency sounds might be detectable at great distances from their source. Many terrestrial animals detect and use low frequency sounds propagated through the air or ground, such as elephants, some desert rodents, and moles. In the marine environment, some pinnipeds, such as the elephant seal, and several mysticete (baleen) whales, such as blue, fin, and right whales, produce and respond to very low frequencies, including infrasonic signals (frequencies below 20 Hz).

Marine mammal sound production is described in How do marine mammals produce sound? Studies on sound generation in pinnipeds are not extensive. It is thought that the primary source of pinniped vocalizations is the larynx as many pinnipeds have vocalization features similar to humans^[1]Ravignani, A., Fitch, W. T., Hanke, F. D., Heinrich, T., Hurgitsch, B., Kotz, S. A., Scharff, C., Stoeger, A. S., & De Boer, B. (2016). What Pinnipeds Have to Say about Human Speech, Music, and the Evolution of Rhythm. Frontiers in Neuroscience, 10. https://doi.org/10.3389/fnins.2016.00274^[2]Spasikova, M., Fitch, W. T., Reichmuth, C., & Schusterman, R. J. (2008). Acoustic production mechanisms in pinnipeds. The Journal of the Acoustical Society of America, 123(5_Supplement), 3771–3771. https://doi.org/10.1121/1.2935383. Pinnipeds that produce very low frequency sounds, like the elephant seal, when on land may produce sounds that are propagated both through the air and through the substrate via contact with their throat and chest^[3]Sanvito, S., Galimberti, F., & Miller, E. H. (2007). Vocal signalling of male southern elephant seals is honest but imprecise. Animal Behaviour, 73(2), 287–299. https://doi.org/10.1016/j.anbehav.2006.08.005.

Baleen whales also use their larynx. These whales have a “u-fold,” which is a thick, u-shaped, ridge of tissue in the larynx. Changes in the u-fold opening, its position and tension, as well as the shape of the laryngeal sac, may alter the frequency and amplitude of sounds produced^[4]Reidenberg, J. S., & Laitman, J. T. (2007). 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), 745–759. https://doi.org/10.1002/ar.20544^[5]Reidenberg, J. S. (2018). Where does the air go? Anatomy and functions of the respiratory tract in the humpback whale (Megaptera novaeangliae). Madagascar Conservation & Development, 13(1), 91. https://doi.org/10.4314/mcd.whales.2.

Marine mammal sound reception is described in How do marine mammals hear. The ability of animals to detect low frequencies depends upon specializations of the outer, middle, and inner ear. Typically, the larger the animal, the better its low frequency hearing. This is true for both marine and terrestrial mammals.

Elephants may detect and discriminate different types of very low frequency and even seismic signals via their large external ears (pinnae) and/or through vibration and pressure sensitive mechanoreceptors in their feet and trunk^[6]Rasmussen, L. E. L., & Munger, B., L. (1996). The sensorineural specializations of the trunk tip (finger) of the Asian elephant, Elephas maximus. Anatomical Record, 246, 127–134..

Mysticetes, similar to low frequency specialized terrestrial mammals, have multiple ear adaptations that enhance low frequency hearing, such as an elongated tympanic membrane that protrudes from the middle ear space (“glove finger”) and a large middle ear cavity. The ear bones are also firmly seated in the skull. Mysticete middle ear ossicles are massive and loosely joined in contrast to the stiff and dense ossicles of the high frequency odontocetes.

As there are no direct audiometric measurements of hearing sensitivities for low frequency cetaceans, estimates of hearing abilities have been made using computer simulations and analyses of how ears operate based on the ear anatomy in multiple species. Such models are tested by comparing results for species for which there are actual audiograms then applying to ears of species that cannot be measured directly. Models have been developed that analyze how differences in middle ear structures affect how acoustic energy is transmitted from the tympanic membrane to the cochlea and how peak resonances of the middle ear cavity relate to best hearing ranges.

Models for minke and humpback whales estimate their best hearing ranges to be between 30 Hz and 7.5 kHz when stimulated at the glove finger, and 100 Hz to 25 kHz for minke whales and 15 Hz to 9 kHz for humpback whales^[7]Tubelli, A. A., Zosuls, A., Ketten, D. R., Yamato, M., & Mountain, D. C. (2012). A prediction of the minke whale ( Balaenoptera acutorostrata ) middle-ear transfer function. The Journal of the Acoustical Society of America, 132(5), 3263–3272. https://doi.org/10.1121/1.4756950^[8]Tubelli, A. A., Zosuls, A., Ketten, D. R., & Mountain, D. C. (2014). Elastic Modulus of Cetacean Auditory Ossicles. The Anatomical Record, 297(5), 892–900. https://doi.org/10.1002/ar.22896.^[9]Tubelli, A. A., Zosuls, A., Ketten, D. R., & Mountain, D. C. (2018). A model and experimental approach to the middle ear transfer function related to hearing in the humpback whale ( Megaptera novaeangliae ). The Journal of the Acoustical Society of America, 144(2), 525–535. https://doi.org/10.1121/1.5048421. These best sensitivity ranges match well with known vocalizations for both species.

The total hearing range for any mammal is determined by the inner ear, specifically by the resonances of the membranes in the cochlea. The cochlear spiral of both elephants and mysticetes has a coil structure that enhances propagation of low frequencies throughout the whole cochlea^[10]Manoussaki, D., Chadwick, R. S., Ketten, D. R., Arruda, J., Dimitriadis, E. K., & O’Malley, J. T. (2008). The influence of cochlear shape on low-frequency hearing. Proceedings of the National Academy of Sciences, 105(16), 6162–6166. https://doi.org/10.1073/pnas.0710037105^[11]Ritsche, I. S., Fahlke, J. M., Wieder, F., Hilger, A., Manke, I., & Hampe, O. (2018). Relationships of cochlear coiling shape and hearing frequencies in cetaceans, and the occurrence of infrasonic hearing in Miocene Mysticeti. Fossil Record, 21(1), 33–45. https://doi.org/10.5194/fr-21-33-2018. The spiral also contains broad basilar membrane capable of responding at extremely low frequencies^[12]Ketten, D. R. (1994). Functional analyses of whale ears: Adaptations for underwater hearing. Proceedings of OCEANS’94, 1, I/264-I/270. https://doi.org/10.1109/OCEANS.1994.363871^[13]Ketten, D. R. (2000). Cetacean Ears. In W. W. L. Au, R. R. Fay, & A. N. Popper (Eds.), Hearing by Whales and Dolphins (Vol. 12, pp. 43–108). Springer New York. https://doi.org/10.1007/978-1-4612-1150-1_2. Based on basilar membrane models, low-frequency hearing for mysticetes extends to 20 Hz, with some species, including fin whales, predicted to hear at infrasonic frequencies as low as 10-15 Hz but also may may reach as high as 30 kHz, for a full hearing range of nearly 12 octaves (Ketten 1994^[14]Ketten, D. R. (1997). STRUCTURE AND FUNCTION IN WHALE EARS. Bioacoustics, 8(1–2), 103–135. https://doi.org/10.1080/09524622.1997.9753356^[15]Parks, S. E., Ketten, D. R., O’Malley, J. T., & Arruda, J. (2007). Anatomical predictions of hearing in the North Atlantic right whale. The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology, 290(6), 734–744. https://doi.org/10.1002/ar.20527^[16]Yamato, M., Ketten, D. R., Arruda, J., & Cramer, S. (2008). Biomechanical and structural modeling of hearing in baleen whales. Bioacoustics, 17(1–3), 100–102. https://doi.org/10.1080/09524622.2008.9753781^[17]Mountain, D. C., Zosuls, A., Newburg, S., & Ketten, D. R. (2008). PREDICTING CETACEAN AUDIOGRAMS. Bioacoustics, 17(1–3), 77–80. https://doi.org/10.1080/09524622.2008.9753772.

High quality descriptions of baleen whale vocalizations are limited and would be helpful for understanding both their significance and what features are important for hearing and hearing models. Acoustic features that may be important include temporal, spectral, and source level characteristics for emitted sounds as well as what received levels correlate with significant observed behavioral responses.

Additional Links on DOSITS

• Animals and Sound > How do marine mammals produce sound?
• Animals and Sound > How do marine mammals hear?
• Animals and Sound > Hearing in land mammals
• Animals and Sound > Hearing in cetaceans and sirenians, the fully aquatic ear
• Animals and Sound > Effects MM > Hearing Loss
• Audio Gallery > Blue Whale
• Audio Gallery > North Atlantic Right Whale
• Audio Gallery > Fin Whale
• Audio Gallery > Humpback Whale
• Audio Gallery > Minke Whale

References

• Heffner, R., & Heffner, H. (1980). Hearing in the Elephant ( Elephas maximus ). Science, 208(4443), 518–520. https://doi.org/10.1126/science.7367876.
• Heffner, R. S., & Heffner, H. E. (1982). Hearing in the elephant (Elephas maximus): Absolute sensitivity, frequency discrimination, and sound localization. Journal of Comparative and Physiological Psychology, 96(6), 926–944.
• Ketten, D. R. (1992). The Marine Mammal Ear: Specializations for Aquatic Audition and Echolocation. In D. B. Webster, A. N. Popper, & R. R. Fay (Eds.), The Evolutionary Biology of Hearing (pp. 717–750). Springer New York. https://doi.org/10.1007/978-1-4612-2784-7_44.
• Ketten, D. R. (2008). Underwater ears and the physiology of impacts: Comparative liability for hearing loss in sea turtles, birds, and mammals. Bioacoustics, 17(1–3), 312–315. https://doi.org/10.1080/09524622.2008.9753860.
• Ketten, D. R., Arruda, J., Cramer, S., & Yamato, M. (2016). Great Ears: Low-Frequency Sensitivity Correlates in Land and Marine Leviathans. In A. N. Popper & A. Hawkins (Eds.), The Effects of Noise on Aquatic Life II (Vol. 875, pp. 529–538). Springer New York. https://doi.org/10.1007/978-1-4939-2981-8_64.
• Park, T., Evans, A. R., Gallagher, S. J., & Fitzgerald, E. M. G. (2017). Low-frequency hearing preceded the evolution of giant body size and filter feeding in baleen whales. Proceedings of the Royal Society B: Biological Sciences, 284(1848), 20162528. https://doi.org/10.1098/rspb.2016.2528.
• Reidenberg, J. S. (2017). Terrestrial, Semiaquatic, and Fully Aquatic Mammal Sound Production Mechanisms. Acoustics Today, 13(2), 35–43.
• Southall, B. L., Finneran, J. J., Reichmuth, C., Nachtigall, P. E., Ketten, D. R., Bowles, A. E., Ellison, W. T., Nowacek, D. P., & Tyack, P. L. (2019). Marine mammal moise exposure criteria: Updated scientific recommendations for residual hearing effects. Aquatic Mammals, 45(2), 125–232. https://doi.org/10.1578/AM.45.2.2019.125.
• Yamato, M., Ketten, D. R., Arruda, J., Cramer, S., & 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, 295(6), 991–998. https://doi.org/10.1002/ar.22459.