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Home , Ear canal, Modiolus (cochlea), Ossicles, Tympanic cavity

Do They Hear What We Hear: Adaptations in for Underwater, Focusing on the Bowhead Whale (Balaena mysticetus)‏

Spring A. Gaines, Hermann H. Bragulla, Daniel J. Hillmann Comparative Biomedical Sciences, School of Veterinary Medicine, Louisiana State University, Baton Rouge, Louisiana

Abstract

The evolution of hearing and how this process occurs has been researched and recorded by scientists for decades. In mammals, different species have developed unique adaptations to be able to capture sounds in their environment. This study focuses on those mammals who live in an aquatic environment, especially cetaceans, whales and dolphins. It is hypothesized that odontocetes (toothed whales) and mysticetes (baleen whales) use their to conduct sound, much like the canal in a human. These mandibles are said to replace the functionality of the . Through observations on the fetal Bowhead whale (Balaena mysticetus) ear done in various media, including gross , CT scanning and schematic drawings, it has been found that not only is conduction through the possible, but other unique adaptations exist as well.

Introduction

Hearing is the process of how sound waves are picked up, transduced and interpreted. This process is performed through the ear, and it can be explained by dividing the ear into three sections. In mammals, the focuses and directs sound waves into the . In the middle ear, the energy of these pressure waves is translated into mechanical vibrations of the middle ear’s bone structure. The of the propagates these mechanical signals as waves in fluid and membranes, and finally transduces them to impulses which are transmitted to the brain. The inner ear is also responsible for balance. This middle ear structure is where sound amplification of 20x occurs (Strain, per. comm.). The middle ear is the portion of the ear internal to the , and external to the vestibular window. The mammalian middle ear (see Fig. 1) contains three , which couple vibration of the eardrum into waves in the fluid and membranes of the inner ear. These three ossicles are called the , , and . The hollow space of the middle ear is called the . In some mammals, there is also a capsule of dense bone partly surrounding the middle ear . This is known as the tympanic bulla (ICVGAN,2005). Sound information can reach the mammalian inner ear through two main routes. Land mammals hear sounds waves that travel though air by vibration. The tympanic membrane and the middle ear ossicles react to these vibrations, which have travelled through the ear canal by helping to produce movement of the vestibular window and changing pressure gradients in the Fig. 12 A-D. Four cross-sectional images taken from spiral CT scans of the fetal Bowhead Whale (Specimen #90B4F). D = Dorsal direction; M = cochlear fluid (Reuter and Nummela, 1998). Medial direction.

A: Rostral-most section through the head of the malleus. Note the fusion of the manubrium of the malleus with the lateral wall of the On the other , mammals that are subterrestial or live tympanic bulla. underwater rely on bone conducted hearing. This is due to the B: Section through the articulation of the incus with the head of the malleus. Note the two and one-half turns of the osseus cochlea and the course of the cochlear part of the eighth cranial nerve (C. N. VIII) within the . difference in environment. There is a smaller acoustical C: Section through the crus of the stapes. Note the base of the stapes inserted into the vestibular window.

D: Caudal-most section through the “glove finger” portion of the tympanic membrane. impedance between the surrounding medium and the body, for earth and water are denser than air. This leads to vibration (Mason, 2001). is also possible in mammals with large ear ossicles (Reuter and Nummela, 1998). Of interest to this study are mammals that live underwater, particularly odontocetes (toothed whales) and mysticetes (baleen whales). While these animals contain an external Results and Conclusion References Acknowledgements ear canal, the end of it is plugged, for the pressure of International Committee on Veterinary Gross Anatomical Nomenclature (2005). water is greater than that of air. To be able to propagate sound Fetal samples were obtained from the North Slope Borough In Bowheads, the tympanic part is attached to the petrous The authors would like to thank Mrs. Cathryn Sparks, Monty in Barrow, Alaska. Through observation of these fetuses, it has part by two bony columns (see Figs. 11a and 11b). Vibration of Nomina Anatomica Veterinaria Fifth Edition. The World Association of Galley and Eric Brooks of the Gross Anatomy Lab for their and interpret its direction and distance, bone conduction must be Veterinary Anatomists: Ithica. 190 pgs. been seen that evidence leading to bone conduction exists. the bulla would cause this entire complex to somehow move, assistance. They would also like to thank Dr. George Strain for possible. A theory is that these animals use their mandibles to Mason, MJ (2001). Middle ear structures in fossorial mammals: a comparison replace the need for the ear canal. In dolphins, a fat pad has There does not appear to be another path for sound. However, in which would influence movement of the cochlear fluid. with non-fossorial species. J. Zool., Lond., 255: 467-486. his communication and insights, comparison with the mandibles of an odontocete, the mysticete Another fusion occurs in the middle ear. In an article by been found in the mandible, and it is thought sound can travel Nummela S, Thewissen JGM, Bajpai S, Hussain T, Kumar K (2007). Sound through this pad to the (See Fig. 2). At this time, does have a significant difference (see Fig. 3). The fat pad does Parks et al. (2007), the malleus is said to be attached to a bony transmission in archaic and modern whales: Anatomical adaptations for not exist. Rather, mysticetes have a vascular rete surrounding strut which is part of the lateral wall of the bulla. In their pictures, underwater hearing. The Anatomical Record, 290: 716-733. it can then travel through the external acoustic meatus, which leads to the tympanic cavity (Nummela et al., 2007). It is the mandibular nerve. This rete could be a drawback for sound one can see the articulation between this strut and the Parks, SE, Ketten, DR, O’Malley, JT, Arruda, J (2007). Anatomical Predictions unknown if this same method is used in mysticetes, This study propagation. manubrium of the malleus. However, the articulation is not found of This poster was made possible by NIH Grant Number P20 Hearing in the North Atlantic Right Whale. The Anatomical Record, will focus on the Bowhead whale to either support or deny this Further research was performed to find if frequency could be in the malleus/strut complex of the Bowhead middle ear. We RR16456 from the INBRE Program of the National Center for the answer. Mysticete calls are at a lower frequency than believe that the entire malleus is fused to the lateral wall (see 290:734-744. Research Resources. Its contents are solely the responsibility of theory. odontocetes. Lower frequencies lead to greater penetration of Figs.11b and 12a), which would cause movement through the Reese CS, Calvin JA, George JC, Tarpley RJ (2001). Estimation of Fetal Growth the authors and do not necessarily represent the official views of Materials and Methods sound (Reidenburg and Laitman, 2007). Knowing this, the ear ossicles if the bulla vibrates. and Gestation in Bowhead Whales. Journal of American Statistical NIH. density of the rete system is no longer a hindrance. This all leads Our final observation compares the adult Bowhead to the Association, 98: 915-923.

Five fetal Bowhead whales were chosen for observation: towards support for the hypothesis. fetal Bowhead. If one takes figures 4-10 in context, one would Reidenberg, JS, Laitman, JT (2007).Discovery of a Low Frequency Sound In addition, the structures within the ear of the Bowhead are see that the ear ossicles and petrous/tympanic complex are Source in Mysticeti (Baleen Whales):Anatomical Establishment of a Vocal one first trimester, two second trimester and two at full term. Fold Homolog. The Anatomical Record, 290:745–759. unique and deserve mention. One finding shows that the ear almost fully developed at the fetal stage, but not ossified. This Cross -sections of two fetal Bowhead whales were dissected to display stages of ear development. They came from the first canal is plugged at one end then opens into a funnel shape. information is crucial to current research being conducted in the Reuter T, Nummela, S (1998). Elephant hearing. Acoustical Society of America. trimester (specimen #92B8F) and one of the second trimester Within this funnel shape is a membrane dubbed the glove finger Beaufort and Chukchi seas of Alaska, which encompass the (specimen #88KK1) fetuses. A schematic was drawn of the (see Figs. 9 and 12d). It is believed that the glove finger acts as migratory path of the Bowhead. Sonic testing and oil drilling are cross-sectioned second trimester fetus. One full term fetus a tympanic membrane. This membrane could help produce being performed in these areas. Over time, this may degrade the ’ (specimen #90B4F) was taken for computed tomography (CT) vibration of the tympanic bulla. If this bulla vibrates, like we whale s hearing and thus its ability to navigate the surrounding scanning in a spiral CT format using protocol. believe, it would in turn vibrate two important structures. environment. All observations were photographed and recorded accordingly.