Do They Hear What We Hear: Adaptations in Mammals for Hearing 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

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 outer ear focuses and directs sound

waves into the middle ear. In the middle ear, the energy of these

pressure waves is translated into mechanical vibrations of the

middle ear’s bone structure. The cochlea of the inner ear

propagates these mechanical signals as waves in fluid and

membranes, and finally transduces them to nerve 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 eardrum, and external to the vestibular

window.

The mammalian middle ear (see Fig. 1) contains three

ossicles, which couple vibration of the eardrum into waves in the

fluid and membranes of the inner ear. These three ossicles are

called the malleus, incus, and stapes. The hollow space of the

middle ear is called the tympanic cavity. 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

cochlear fluid (Reuter and Nummela, 1998).

On the other hand, mammals that are subterrestial or live

underwater rely on bone conducted hearing. This is due to the

difference in environment. There is a smaller acoustical

impedance between the surrounding medium and the body,

for earth and water are denser than air. This leads to skull

vibration (Mason, 2001). Bone conduction 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

ear canal, the end of it is plugged, for the pressure of

water is greater than that of air. To be able to propagate sound

and interpret its direction and distance, bone conduction must be

possible. A theory is that these animals use their mandibles to

replace the need for the ear canal. In dolphins, a fat pad has

been found in the mandible, and it is thought sound can travel

through this pad to the temporal bone (See Fig. 2). At this time,

it can then travel through the external acoustic meatus, which

leads to the tympanic cavity (Nummela et al., 2007). It is

unknown if this same method is used in mysticetes, This study

will focus on the Bowhead whale to either support or deny this

theory.

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 mandibles to conduct sound, much like the

ear canal in a human. These mandibles are said to replace the

functionality of the ear canal. Through observations on the fetal

Bowhead whale (Balaena mysticetus) ear done in various media,

including gross anatomy, CT scanning and schematic drawings,

it has been found that not only is bone conduction through the

mandible possible, but other unique adaptations exist as well.

Materials and Methods

Five fetal Bowhead whales were chosen for observation:

one first trimester, two second trimester and two at full term.

Cross-sections of two fetal Bowhead whales were dissected to

display stages of ear development. They came from the first

trimester (specimen #92B8F) and one of the second trimester

(specimen #88KK1) fetuses. A schematic was drawn of the

cross-sectioned second trimester fetus. One full term fetus

(specimen #90B4F) was taken for computed tomography (CT)

scanning in a spiral CT format using human brain protocol.

All observations were photographed and recorded accordingly.

Results and Conclusion

Fetal samples were obtained from the North Slope Borough

in Barrow, Alaska. Through observation of these fetuses, it has

been seen that evidence leading to bone conduction exists.

There does not appear to be another path for sound. However, in

comparison with the mandibles of an odontocete, the mysticete

does have a significant difference (see Fig. 3). The fat pad does

not exist. Rather, mysticetes have a vascular rete surrounding

the mandibular nerve. This rete could be a drawback for sound

propagation.

Further research was performed to find if frequency could be

the answer. Mysticete calls are at a lower frequency than

odontocetes. Lower frequencies lead to greater penetration of

sound (Reidenburg and Laitman, 2007). Knowing this, the

density of the rete system is no longer a hindrance. This all leads

towards support for the hypothesis.

In addition, the structures within the ear of the Bowhead are

unique and deserve mention. One finding shows that the ear

canal is plugged at one end then opens into a funnel shape.

Within this funnel shape is a membrane dubbed the glove finger

(see Figs. 9 and 12d). It is believed that the glove finger acts as

a tympanic membrane. This membrane could help produce

vibration of the tympanic bulla. If this bulla vibrates, like we

believe, it would in turn vibrate two important structures.

Acknowledgements

The authors would like to thank Mrs. Cathryn Sparks, Monty

Galley and Eric Brooks of the Gross Anatomy Lab for their

assistance. They would also like to thank Dr. George Strain for

his communication and insights,

This poster was made possible by NIH Grant Number P20

RR16456 from the INBRE Program of the National Center for

Research Resources. Its contents are solely the responsibility of

the authors and do not necessarily represent the official views of

NIH.

References

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Nomina Anatomica Veterinaria Fifth Edition. The World Association of

Veterinary Anatomists: Ithica. 190 pgs. Mason, MJ (2001). Middle ear structures in fossorial mammals: a comparison with non-fossorial species. J. Zool., Lond., 255: 467-486. Nummela S, Thewissen JGM, Bajpai S, Hussain T, Kumar K (2007). Sound transmission in archaic and modern whales: Anatomical adaptations for underwater hearing. The Anatomical Record, 290: 716-733.

Parks, SE, Ketten, DR, O’Malley, JT, Arruda, J (2007). Anatomical Predictions

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Reese CS, Calvin JA, George JC, Tarpley RJ (2001). Estimation of Fetal Growth

and Gestation in Bowhead Whales. Journal of American Statistical

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Reidenberg, JS, Laitman, JT (2007).Discovery of a Low Frequency Sound Source in Mysticeti (Baleen Whales):Anatomical Establishment of a Vocal Fold Homolog. The Anatomical Record, 290:745–759.

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In Bowheads, the tympanic part is attached to the petrous

part by two bony columns (see Figs. 11a and 11b). Vibration of

the bulla would cause this entire complex to somehow move,

which would influence movement of the cochlear fluid.

Another fusion occurs in the middle ear. In an article by

Parks et al. (2007), the malleus is said to be attached to a bony

strut which is part of the lateral wall of the bulla. In their pictures,

one can see the articulation between this strut and the

manubrium of the malleus. However, the articulation is not found

in the malleus/strut complex of the Bowhead middle ear. We

believe that the entire malleus is fused to the lateral wall (see

Figs.11b and 12a), which would cause movement through the

ear ossicles if the bulla vibrates.

Our final observation compares the adult Bowhead to the

fetal Bowhead. If one takes figures 4-10 in context, one would

see that the ear ossicles and petrous/tympanic complex are

almost fully developed at the fetal stage, but not ossified. This

information is crucial to current research being conducted in the

Beaufort and Chukchi seas of Alaska, which encompass the

migratory path of the Bowhead. Sonic testing and oil drilling are

being performed in these areas. Over time, this may degrade the

whale’s hearing and thus its ability to navigate the surrounding

environment.

Fig. 12 A-D. Four cross-sectional images taken from spiral CT scans of the fetal Bowhead Whale (Specimen #90B4F). D = Dorsal direction; M = 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 tympanic bulla. 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 modiolus. 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.