The effect of craniokinesis on the middle ear of domestic chickens (Gallus gallus domesticus)

Abstract

The avian middle ear differs from that of mammalians and contains a tympanic membrane, one ossicle (bony columella and cartilaginous extra-columella), some ligaments and one muscle. The rim of the eardrum (closing the middle ear cavity) is connected to the neurocranium and, by means of a broad ligament, to the otic process of the quadrate. Due to the limited number of components in the avian middle ear, the possibilities of attenuating the conduction of sound seem to be limited to activity of the stapedius muscle. We investigate to what extent craniokinesis may impact the components of the middle ear because of the connection of the eardrum to the movable quadrate. The quadrate is a part of the beak suspension and plays an important role in craniokinesis. Micro-computed tomography was used to visualize morphology and the effect of craniokinesis on the middle ear in the domestic chicken (Gallus gallus domesticus). Both hens and roosters are considered because of their difference in vocalization capacity. It is hypothesized that effects, if present, of craniokinesis on the middle ear will be greater in roosters because of their louder vocalization. Maximal lower jaw depression was comparable for hens and roosters (respectively 34.1 ± 2.6° and 32.7 ± 2.5°). There is no overlap in ranges of maximal upper jaw elevation between the sexes (respectively 12.7 ± 2.5° and 18.5 ± 3.8°). Frontal rotation about the transversal quadrato-squamosal, and inward rotation about the squamosal-mandibular axes of the quadrate were both considered to be greater in roosters (respectively 15.4 ± 2.8° and 11.1 ± 2.5°). These quadrate rotations did not affect the columellar position or orientation. In hens, an influence of the quadrate movements on the shape of the eardrum could not be detected either; however, craniokinesis caused slight stretching of the eardrum towards the caudal rim of the otic process of the quadrate. In roosters, an inward displacement of the conical tip of the tympanic membrane of 0.378 ± 0.21 mm, as a result of craniokinesis, was observed. This is linked to a flattening and slackening of the eardrum. These changes most likely go along with a deformation of the extra-columella. Generally, in birds, larger beak opening is related to the intensity of vocalization. The coupling between larger maximal upper jaw lifting in roosters and the slackening of the eardrum suggest the presence of a passive sound attenuation mechanism during self-vocalization.

Keywords: chicken; craniokinesis; micro-CT; middle ear; quadrate.

Figure 1

Chicken skull and quadrate morphology. (A) Surface model of skull, lateral view. Red: quadrate; black dashed line: axis of skull removal. (B) Surface model of left quadrate (red), tympanic membrane (purple) and broad ligament (green) connecting the quadrate (between c and d) and tympanic membrane (between a and b). The rest of the tympanic membrane is connected to the neurocranium. (C) Middle ear components: tympanic membrane (purple), extra‐columella (green) and columella (blue).

Figure 2

Morphology of hen skull with closed (purple) and open beak (red). α: lower jaw depression; β: upper jaw elevation; Position of the four‐bar system when the beak is closed is depicted in full lines. Position of the four‐bar system when the beak is opened is shown with dashed lines. (A) crank; (B) coupler; (C) rocker; (D) frame.

Figure 3

Axes about which the quadrate rotation angles are calculated. Directionality is indicated by the rotational arrows. (A) Frontal rotation of the quadrate about the quadrato‐squamosal axis (Q‐S axis; red). (B) Lateral view of quadrate and (C) frontal view of quadrate: axial rotation about the squamosal‐mandibular axis (S‐M axis; green).

Figure 4

Measurements of upper jaw elevation and lower jaw depression. Green: hen; red: rooster.

Figure 5

Surface models of the aligned left quadrates of one hen (green) and one rooster (red) after scaling. (A) Lateral view; (B) frontal view.

Figure 6

Measurements of frontal rotation of the quadrate about the quadrato‐squamosal axis (Q‐S axis) and rotation angle of the quadrate about the squamosal‐mandibular axis (S‐M axis). Green: hen; red: rooster.

Figure 7

Position of the columella: (A) lateral and (B) top view of the columella of one hen and (C) lateral and (D) top views of the columella of one rooster with closed beak (green) and open beak (red). Position of the extra‐columella (blue) on the columella in hen with closed beak (same orientation on columella of rooster, but not shown in Figure).

Figure 8

Color code: green: closed beak, red: maximal beak opening. (A) Edge on view of the left tympanic membrane of a hen. (B) Oblique view of the left tympanic membrane of a hen. (C) Edge on view of the left tympanic membrane of a rooster. (D) Oblique view of the left tympanic membrane of a rooster.

Figure 9

Schematic overview of the tympanic membrane and the otic process of the quadrate bone (A) in hens and (B) in roosters. Purple: tympanic membrane; green: quadrate positon closed beak; red dotted line: quadrate position open beak; purple star: position of conical tip of tympanic membrane; green dot: position of beads with closed beak; red plus: position of beads with opened beak; black arrows: direction of beads (tympanic membrane) displacements (tension) (NOT magnitude of displacement).