Structure of the external auditory meatus of the Bowhead whale (Balaena mysticetus) and its relation to their seasonal migration

Abstract

The external auditory meatus (EAM) in many species of mysticete whales is filled with a waxy ear plug. Though this lamellated structure is often used to age a whale, its formation and development remain undescribed. It is thought that growth layer groups (GLGs) are laid down annually, thereby increasing the size of this structure. Since some mysticete whales are migratory and many undergo molting, we hypothesized that the cyclical production of these GLGs may be related to these processes. The epithelia of both EAM and glove finger (a part of the tympanic membrane protruding into the EAM) of one juvenile and multiple adult bowhead whales from both fall (October: non‐molting) and spring (May: molting) seasons were dissected and examined anatomically and histologically. These tissue samples were compared with the adult oral epithelia at the same time periods. These epithelia shared a similar basic broad structure, though there were differences in thickness and presence of intraepithelial structures. All epithelia in the October specimens were rich in both glycogen and lipid. The parakeratinized epithelium of the oral cavity in the juvenile and some May specimens shed via the production of several superficial epithelial fissures. Other adult May specimens exhibited deep epithelial fissures, reminiscent of pressure ulcers, which would cause the detachment of the entire epithelium from the dermis. We propose that sloughed epithelial lining is the source of the GLGs in the ear plug. Correlating a potential molting sequence with these observations explained the presence of epidermal glycogen, deep epidermal fissures and dermal glycolipid, and to some extent calls into question the origin and structure of the ear plug itself. Further morphological characterization of ear plugs in bowheads is needed to better understand cell origin and ear plug formation.

The role of desmosomes in the ear plug formation in the bowhead whale (Balaena mysticetus)

“…The fall samples show that no skin is shed in this season, as the epithelium has three distinct layers and lacks fissures. Whether epidermal growth is complete or partially complete remains to be resolved, though the presence of intracellular glycogen in the keratinocytes (Rehorek et al, 2019) and ample dsg1 and dsc1 between keratinocytes suggests that epidermal differentiation may still be taking place (Getsios et al, 2009). This may account for the presence of dsc1 and dsg1 in the stratum basale of whale epithelial tissue (both oral cavity and EAM).…”

“…(a) The opening of the EAM on the surface of the head is closed or so narrow (Ketten, 1997) that no exudate passes out of the EAM, and this leads to a build‐up of material within the EAM. This build‐up consists of an “ear‐plug” which consists of a series of concentric rings of waxy substances (see Rehorek et al, 2019 for review). (b) There are neither ceruminous nor sebaceous glands in the EAM (Ichihara, 1959; Rehorek et al, 2019), and thus only skin is periodically shed into the lumen.…”

“…This build‐up consists of an “ear‐plug” which consists of a series of concentric rings of waxy substances (see Rehorek et al, 2019 for review). (b) There are neither ceruminous nor sebaceous glands in the EAM (Ichihara, 1959; Rehorek et al, 2019), and thus only skin is periodically shed into the lumen. The parakeratinized epithelium is shed entirely, via the formation of annual deep intraepithelial and subepithelial fissures (Rehorek et al, 2019).…”

“…Thus, there is no corresponding laminated ear wax accumulation (Thewissen unpublished observation). However, the regeneration of the epithelium only takes a few months (Rehorek et al, 2019). Since the epidermis is intact for most of the year, an active mechanism must be in place for it to be shed in the spring.…”

Diseases and parasites

“…Seasonal skin molting as reported for three bowhead whale stocks (OKS, Chernova et al, 2016 ; Eastern Canada-West Greenland, Fortune et al, 2017 ; BCB, Rehorek et al, 2019 ) could provide a regulatory mechanism for shedding cyamids, epizoic diatom, as well as photo-damaged skin ( Martinez-Levasseur et al, 2013 , Shpak and Stimmelmayr, 2017 ).…”