73 Hearing Research, 13 (1984) 73-76 Elsevier

HRR 00449

Notes on the comparative mechanics of hearing. I. A shock-proof ear

L.U.E. Kohlbffel Institut fiir Physiologic und Biokybernetik, Universitiit Erlangen - Niirnberg, Universitiitsstr. I7, 8520 Erlangen, F. KG.

(Received 11 July 1983; accepted 21 November 1983)

In woodpeckers, the cochlear windows show functional specialization. The small membrane of the round window is attached to a special bony plate of the columella. This arrangement of coupled windows probably increases power dissipation at the fenestral

boundaries and so dampens impulsive mechanical disturbances.

woodpecker, ear protection, bone conduction

Introduction

The ear is sensitive to small amounts of mecha- nical energy. How does it cope with the energy released suddenly in mechanical shock? In wood-

peckers [l-5,10,11,13,14] one might expect to find special features for ear protection. In pecking,

collision exchange with the substrate could cause bone-conducted mechanical transients in the audi- tory range. Rapid skull deceleration on impact and impact-induced bone vibration could lead to ex- cessive ossicular excursions and shock wave for- mation in cochlear fluids. This report describes the functional specialization at the cochlear windows observed in woodpeckers.

Methods

The otic region and the inner ear of many birds were dissected to discover common and variant features in avian gross cochlear morphology: goose,

northern mallard, partridge; common quail, domestic turkey, guinea fowl, domestic cock,

pheasant, domestic pigeon, tawny owl, blackbird, coal-titmouse, nuthatch, wood-wren; Piciformes: toucan - Ramphastus taco (2, x), green wood-

pecker - Picus viridis (3, x), grey-headed wood- pecker - Picus cunw (1, x), black,woodpecker - Dryocopus martius (2, x), great spotted woodpecker - Dendrocopus major (3 nestlings, 3 adult birds).

0378-5955/84/$03.00 0 1984 Elsevier Science Publishers B.V.

(In parentheses are given the number of speci- mens; an x indicates that dried specimens ob- tained from zoological collections were examined). Preparations were fixed and stored in 10% for- malin solution. Dissection was done under the stereomicroscope. Drawings are by the author.

Results and Discussion

In woodpeckers, specialization is in the recessus

stapedialis at the cochlear windows *. The stape- dial recess is narrow and its opening towards the middle ear cavity is just wide enough for the handle of the columella to pass through (Fig. la). The oval window has the usual area, but the round window has less than half the usual area. The specially narrow round window roofs over the anterior and posterior part of the oval window. The trabeculated, light-weight columella has two footplates. The usual ovoid vestibular plate fits the oval window and faces Scala vestibuli (cisterna scalae vestibuli). The special trapezoidal tympanic plate faces the recessus scalae tympani (Fig. lb). The pattern of trabeculation of the columella shows

l The orientation of the ear in the skull is similar to other birds. Eardrum, extracohtmella, middle ear muscle, cochlear aquaeduct, hehcotrema, ductus brevis, basilar and tectorial membrane do not show specializations in woodpeckers as seen under the stereomicroscope.

a b , lmm ,

Fig. 1. Stapedial recess in the black woodpecker - Dryocopur

martins (left ear, round window membrane removed). (a) Outer view of the narrow recess which closely surrounds the handle of

columella (extracolumella removed). (b) View from the opened

recessus scalae tympani into the stapedial recess through the

round window. The tympanic plate of the columella faces the narrow round window. C, columella; TP, tympanic plate of

columella; IFP, interfenestral process; RST, recessus scalae

tympani; an, anterior; me, medial; do, dorsal.

intra- and interspecies variation. But the dual-plate columella (Fig. 2) and the narrow round window are osteological features common to all four species examined, in spite of the differences in hacking habits between the black and great spotted wood- pecker (‘Baum-, Hackspechte’) and the green and grey-headed woodpecker (‘Bodenspechte’) *.

The perilymphatic space at the round window is sealed by the tympanic face of the columella and the membrane of the round window (membrana tympani secundaria). The membrane connects to the perimeter of the tympanic plate. As seen in preparations of the great spotted woodpecker, the membrane is small and it has a steep thickness gradient: close to the tympanic plate it is thin, and towards the roof of the recessus scalae tympani it is very thick (Fig. 3). Morphogenetically the char- acteristic features of the stapedial recess form early

* The picture of the columella of the green woodpecker by **In parrots [6,12] and the nuthatch (S&a europaa, own

Krause ([9], Taf. 2, No. 17) is misleading. It does not show observations) the round window membrane also has a steep

the tympanic plate and portrays the handle of the columella thickness gradient. In the toucan the round window mem-

as too massive. brane is attached to a bony ridge of the columella [g].

lmm ,

Fig. 2. The piciform columella has two footplates: the usual ovoid vestibular plate and the special trapezoidal tympanic

plate. (a) Black woodpecker - Dryocopw murrius (right col- umella), (b) great spotted woodpecker - Dendrocopur major

(right), (c) green woodpecker - Picus oiridis (right), (d) grey-

headed woodpecker - Picus canus (left). VP, vestibular plate; TP, tympanic plate of columella.

in development. The typical features are found complete in young nestlings with the labyrinthine bone still thin and soft (ca. 14 days after hatching) * *.

The attachment of the round window mem- brane to the tympanic plate impairs the vibration of the columella. Force is required to stretch the membrane, and the force is the greater the smaller and thicker the membrane and the longer the border line with the tympanic plate. Owing to the

a dO&A

RWM /

. YP

Fig. 3. The membrane of the round window is attached at the circumference of the tympanic plate of the columella (great

spotted woodpecker - Dendrocopus major, left ear). (a) Window

configuration seen from outside (stapedial recess opened; ex-

tracolumella partly shown). (b) Round window membrane in

section (inner ear opened, extracolumella removed). RWM,

round window membrane; AL, annular ligament; VP and TP,

vestibular and tympanic plate of columella; CSV, cistema

scalae vestibuh; RST, recessus scalae tympani; an, anterior; me, medial; do, dorsal.

thickness gradient, membrane strain is concentrat- ed in the thin part close to the columella. Here the membrane is soft as noticed by testing with a static point-load (hair-probe). Little elastic force is transmitted to the tympanic plate since membrane deformation does not noticeably displace col- umella, extracolumella and eardrum. Thus the elastic restoring forces of the middle ear transmis- sion system appear little changed by window cou- pling. It is likely, however, that the frictional force at the window is increased due to viscous shear stress. The smaller and narrower the membrane and the steeper its thickness gradient the steeper are the velocity gradients in the membrane and the greater are the viscous shear stresses during vibra- tion. So the coupling probably increases frictional resistance and power dissipation at the co&ear

windows - the vestibular and tympanic faces of

the columella footplate have about equal areas in contact with perilymph. If the mode of ossicular

motion was a rotational vibration with the inter- fenestral process as axis of rotation, the cochlear fluid would be driven in a fully re-entrant mode. (Re-entrant fluid circuits have been described in several reptilian ears [l&16].) However, as in other birds, the columella in woodpecker is constrained by the suspension system of the extracolumella to

move in a translational mode whose axis coincides with the handle of the columella and is normal to the plane of the oval window. (At least so it is seen

when the eardrum is statically displaced.) Thus the

fluid circuit is only partially re-entrant: the volume displacement of the round window membrane I’,,

is smaller than the volume displacement of the oval window Vow since V,, = Va, + Van, with

V,, as the re-entrant fluid volume. The functional significance of the coupled flow fields at the windows is unclear. Flow coupling through partial re-entrance may reduce the resultant transient force acting on the sound conducting system in the condition of mechanical shock.

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