Morphological study of the upper, lower and third eyelids in the African black ostrich (Struthio camelus camelus L., 1758) (Aves: Struthioniformes) during the embryonic and postnatal period

Abstract

The upper, lower and third eyelids are accessory organs of the eye. The aim of this study was to describe the development of the upper, lower and third eyelids in ostriches in the embryonic and postnatal period and to characterise the conjunctivaassociated lymphoid tissue (CALT) in the eyelids. The study was performed on 59 African black ostriches from the 28 th day of incubation up to 3 years of age. Hematoxylin and eosin, Azan trichrome, van Gieson trichrome and Mallory's trichrome stainings were used to demonstrate the structure of the eyelids. The connective tissue structure transformed from loose connective tissue into dense connective tissue during the development of the eyelids. In the third eyelid, the network of collagen fibres was rebuilt and the density of the collagen fibres decreased with age. As the animals grew, there were clearly visible changes in the structure of the upper and lower eyelids, especially in the stratified squamous epithelium of the skin surface, the conjunctival epithelium and the tarsal plate. The lymphatic follicles were observed only in the lower eyelid of adult ostriches. A diffuse CALT system with scattered lymphatic cells was observed within the connective tissue of the third eyelid, mostly under the conjunctival epithelium in the group of adult birds.

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

“…The upper and lower eyelids are dermomuscular folds that surround the palpebral fissure. 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 mammalian third eyelid moves passively, whereas in birds it moves actively due to the presence of two muscles—the quadratus third eyelid muscle ( m. quadratus membranae nictitans ) and the pyramidal third eyelid muscle ( m. pyramidalis membranae nictitans ). The role of the third eyelid is to protect, moisten and clean the cornea (Hall et al., ; Klećkowska‐Nawrot, Goździewska‐Harłajczuk, et al., ; Klećkowska‐Nawrot, Nowaczyk, et al., ; Nomina Anatomica Avium, ). The free margins of the third eyelid possess characteristic thick folds, which enable the removal of fluids and detritus from the corneal surface (Klećkowska‐Nawrot, Goździewska‐Harłajczuk, et al., ; Nomina Anatomica Avium, ).…”

“…In mammals and birds, the ocular surface is protected from different bacterial, viral and toxic infections (which cause conjunctivitis), allergic factors and dry‐eye syndrome by lymphoid tissue, which forms the conjunctiva‐associated lymphoid tissue (CALT) (Oria et al., ; Siebelmann et al., ). The CALT contains antigen‐specific immunoglobulin A (IgA)‐secreting plasma cells and cytokine‐producing T and B‐cells, which are very important in maintaining ocular immunity (Fix & Arp, ; van Ginkel et al., ; Klećkowska‐Nawrot, Goździewska‐Harłajczuk, et al., ). In mammals, the CALT forms the head‐associated lymphoid tissue (HALT) and constitutes the eye‐associated lymphoid tissue (EALT) (Fix & Arp, ; van Ginkel et al., ; Klećkowska‐Nawrot, Goździewska‐Harłajczuk, et al., ; Knop & Knop, , , , , ; Nasrin, Khan, Siddiqi, & Masum, ; Paulsen, Paulsen, Thale, Schaudig, & Tillmann, ).…”

“…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., ).…”

“…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., ). In birds, the CALT is present within the conjunctival fornix of the lower eyelids and the ocular epithelium of the third eyelid (Fix & Arp, ).…”