Histological and Ultrastructural Studies on the Conjunctiva of the Barred Owl (Strix varia)

Abstract

This report is the first characterization of the histology and ultrastructure of the barred owl conjunctiva. The inferior eyelid was dominated by a large disk-shaped plate covered by a non-keratinized stratified squamous or cuboidal epithelium of variable thickness. The apical surface of the plate epithelium varied from flat to long microvilli or even short cytoplasmic extensions similar to those seen in the third eyelid. All specimens had a few goblet cells filled with mucous secretory granules in the plate region. The underlying connective tissue was a dense fibroelastic stroma. Eosinophils were surprisingly common in the epithelial layer and underlying connective tissue in the plate and more distal orbital mucosal region. The orbital mucosa contained goblet cells with heterogeneous glycosylation patterns. The leading edge and marginal plait of the third eyelid are designed to collect fluid and particulate matter as they sweep across the surface of the eye. The palpebral conjunctival surface of the third eyelid was covered by an approximately five-cell-deep stratified squamous epithelium without goblet cells. The bulbar surface of the third eyelid was a bilayer of epithelial cells whose superficial cells have elaborate cytoplasmic tapering extensions reaching out 25 μm. Narrow cytofilia radiated outwards up to an additional 15–20 μm from the cytoplasmic extensions. Lectin labeling demonstrated heterogeneous glycosylation of the apical membrane specializations but only small amounts of glycoprotein-filled secretory granules in the third eyelid.

The differences in the eyelids microstructure and the conjunctiva‐associated lymphoid tissue between selected ornamental and wild birds as a result of adaptation to their habitat

“…() in the adult African black ostrich and the Bilgorajska goose, the stroma of the upper and lower eyelids was composed of a dense connective tissue with densely packed collagen fibres and fibrocytes. In all of the examined birds, there were more or less numerous clusters of melanocytes, which were present, either only in the marginal zone or in all of the eyelid areas, as in the Barred owl (Jochems & Phillips, ). According to Klećkowska‐Nawrot, Goździewska‐Harłajczuk, et al.…”

“…There are few studies focusing on the eyelid morphology and CALT development in wild and ornamental birds, which inhabit homes, zoos and wildlife shelters. The eyelid anatomy has been described in the English sparrow, pigeon, common buzzard, hooded merganser, rockhopper penguin, common mallard, falcon, hawk, vulture, chicken, turkey, barred owl, Bilgorajska goose and African black ostrich (Bacha & Bacha, ; Bielek, ; Gultiken et al., ; Jochems & Phillips, ; Klećkowska‐Nawrot, Goździewska‐Harłajczuk, et al., ; Klećkowska‐Nawrot, Nowaczyk, et al., ; Kolmer, ; Kühnel & Schramm, ; NAA, ; Sivak & Glover, ; Wood, ). Our study revealed large variation in the anatomy of the upper and lower eyelid in the studied bird supraorders.…”

“…(), the tarsal plate in the adult African ostrich was thick and consisted of a dense connective tissue containing elastic fibres and single large blood vessels. According to Jochems and Phillips (), the tarsal plate in the barred owl was a large, oval fibrous slightly elevated disc.…”

“…In birds, both eyelids protect the eye from injury and control the amount of light entering the eye through opening and closing of the palpebral fissure (Klećkowska‐Nawrot, Goździewska‐Harłajczuk, & Nowaczyk, ; Nickel, Schummer, & Seiferle, ). The eyelids in birds consist of three layers: unfeathered skin or skin covered by delicate feathers, a middle musculofibrous layer containing the m. levator palpebrae dorsalis and m. depressor palpebrae ventralis , sebaceous glands (Zeis glands) and ciliary sweat glands (Moll's gland), as well as a mucous membrane, known as the palpebral conjunctiva with goblet cells (Bacha & Bacha, ; Gultiken, Onuk, Karayigit, & Yildiz, ; Jochems & Phillips, ; Nickel et al., ; Nomina Anatomica Avium, ). The upper eyelid in birds is short and thick, whereas the lower eyelid is longer, thinner and very moveable.…”

“…In birds, the CALT is assumed to play a key role in the protection of the eyes by initiating and regulating immune responses as well as participating in the mucosal immunity of the nasopharynx (Khan et al., ; Seo et al., ; Siebelmann et al., ; Steven & Gebert, ; Steven et al., ). In mammals, the lacrimal apparatus and CALT moisturize the eye and supply the cornea and superior and inferior conjunctival sacs with nutrients and antibodies to maintain their health (Dartt, ; Jochems & Phillips, ; Klećkowska‐Nawrot, Goździewska‐Harłajczuk, et al., ; Klećkowska‐Nawrot, Nowaczyk, et al., ; Maggs, ). In humans, the CALT is present in the form of organized lymphoid follicles and diffuse lymphoid tissue (lymphocytes and plasma cells) located in the upper and lower eyelids (Klećkowska‐Nawrot, Goździewska‐Harłajczuk, et al., ; Knop & Knop, ; Siebelmann et al., ).…”