Discussion
The black-winged kite (Elanus caeruleus ), also known as the black-shouldered kite, is a small diurnal prey-predator bird. In 1987, Jaksic studied the behavior of this bird and concluded that the changes in food requirements (breeding and nonbreeding) were met entirely by changes in hunting yield. The visual acuity of these kites is one of the important tools in the hunting process (Potier, 2020).
The present study observed a modified filoplume feathers spars on the skin of the lower eyelid and a collection of copious plumage at the anterior side of the eye, similar results had been observed by (Mahmoud et al. 2022) in Little Owl and (Jochems & Phillips, 2015) in Barred Owl. Anatomically, the feather near the eyelid is characterized by the absence of a vane. This type of modification protects the eye from ultraviolet radiation injury and prevents the adhesion of food and dust particles during feeding and fighting. (Mendelsohn,1983) pointed out that soft feathers can adhere with some grass seeds, whilst a long and wide bony shelf protected the upper eyelid which lack feather. Also, the unfeathered areas have a much denser supply of blood vessels than skin in feathered areas (Negro et al. 2006). This explains the high vascularization in the thick skin of the upper eyelid and the palpebral margins of both eyelids of the black-winged kite.
Elanus caeruleus possesses a thin lower eyelid with feathers, and the movement observation recorded that the lower lid moved more than the upper. Those observations explain the role of the lower eyelid in the protection of the eye against ultraviolet radiation injury when closed. (Knop et al. 2010 and 2011) pointed out the feather follicles provide the epithelial stem cells that help repair wounds, as well as, the thick skin in the marginal region provides protection to areas that experience more friction and abrasion.
The present study demonstrated the presence of Langerhans cells in the skin of the upper and lower eyelids. Langerhans cell in Elanus caeruleus increases in number in the lid margin. Langerhans cells serve as “sentinels” at the interface of the external environment and the immune system, and it bridges aspects of the innate (skin) and adaptive (T cells) immune responses (Neagu et al. 2022). They are stellate cells that protrude their dendrites via tight junctions toward the stratum corneum and as such can probe for antigens across several layers of the epidermis without disrupting the permeability barrier (Deckers et al. 2018).
The present study observed the presence of M like cells in the different parts along the conjunctiva surface of both eyelids of Elanus caeruleus and the nictitating membrane and associated with the surfaces facing the eye fornices. Similar results were recorded in fowl and turkey, which also were similar in many respects to those found in mammals (Maxwell et al. 1986). (Fix & Arp, 1989) referred to the association of M-like cells with the underlying lymphoid tissue in the turkey CALT epithelium. (Oya et al. 2021) also observed the presence of the M like cell in the tear duct-associated lymphoid tissue (TALT) and suggested that it may contribute to immune surveillance in the eye region because of their uptake capacity of the luminal nanoparticles.
The MCJ of the marginal region of the lower eyelid of Elanus caeruleus is composed of nine layers of non-keratinized stratified squamous epithelium with scattered single mucous cells which does not found in the margin of the upper eyelid. (Knop et al. 2011) mentioned the presence of goblet cells in human lid margin the goblet cells regularly occurred either as single cells or arranged into groups. The goblet cells were also observed in the conjunctiva of the upper and lower eyelid and the nictitating membrane of Elanus caeruleus. The goblet cells are essential components of the conjunctival mucosal immune system and they produce immune-regulatory factors, such as TGF- β215 and retinoic acid (RA) (Xiao et al. 2018; Gipson, 2016; Gipson et al. 2014). They mentioned the function of the goblet cell, whereby mucin maintains ocular surface hydration, stabilizes tears and removes pathogens and debris.
The conjunctival epithelium differed between the non-lymphoid and lymphoid regions, where the non-lymphoid conjunctiva is covered by a stratified columnar epithelium containing goblet cells, while in lymphoid regions; the epithelium does not contain goblet cells, and aggregation of the solitary lymphoid follicles (Kageyama et al. 2006; Bayraktaroglu et al. 2011). The present histological and scanning electron microscopy investigations of Elanus caeruleus showed the different distributions of goblet cells and of lymphoid follicles aggregations in the eyelids. Numerous goblet cells varying in size are localized in the conjunctival epithelium of the lower eyelid close contact with lymphatic aggregation near the tarsal plate
Some animals were similar to Elanus caeruleus, such asChinchilla lanigera (Voigt et al. 2012) and guinea pigs (Gasser et al. 2011), where numerous goblet cells appeared in the bulbar and palpebral conjunctiva zone, and occasional goblet cells in lymphoid regions in the upper and lower eyelid.
The distribution of the lymphoid follicles differs between different families and species such as in chicken, it was observed the lymphoid follicles in the upper eyelid are much smaller and are located near the lacrimal ducts (Van Ginkel et al. 2012). Whereas, (Franklin & Remus, 1984) indicated the presence of diffuse lymphocytes in the rabbit eye. (Klećkowska-Nawrot, Nowaczyk, et al. 2016) observed that the human conjunctiva contains lymphoid follicles in both the lower and upper eyelid, on the other side, rodents (such as rats and mice) do not contain lymphoid follicles under physiological conditions, and have very few diffusely interspersed lymphoid cells.
The lymphatic cell aggregation observed in Elanus caeruleus were present only in the lower eyelid and were small compared with those in other animal species studied by (Chodosh et al. 1998). We noticed them under the conjunctival epithelium near the tarsal plate, as well as, the Phoenicopterimorhae and Procellariimorphae, examined by (Klećkowska-Nawrot, Nowaczyk, et al. 2017), whereas in the Strigimorphae solitary lymphoid follicles were located under the tarsal plate.
The lymphoid follicles contain a heterogeneous population of lymphocytes within the conjunctival folds and fissures of the avian lower eyelid (Fix & Arp, 1991). In the adult African black ostriches, the aggregation of lymphoid follicles were observed mostly in the lower eyelid, however, in the upper eyelid, they were limited to the nasolacrimal punctum (Bayraktaroglu et al. 2011).
The present study revealed that the conjunctiva-associated lymphoid tissue in the eyelid of Elanus caeruleus consists of the intraepithelial lymphocytes, subepithelial lymphoid cells and blood vessels. The diffuse CALT was also located within the conjunctival folds under the conjunctival epithelium, similar results were observed in ostriches by ( Klećkowska-Nawrot et al. 2016). Lymphocytes from the bloodstream pass to the lymphoid tissue principally via specialized high endothelial venules (HEV).
However, the present investigations revealed that the diffuse lymphoid tissue of lymphocytes (predominantly T cells), B lymphocytes and plasma cells formed a thin layer in the lamina propria of the conjunctiva, and around the high endothelial venules (HEV) distributed along the lower eyelid and increased in the palpebral margins while in the upper eyelid restricted in the marginal region. In humans, HEV are located in diffuse lymphocytes and lymphoid follicles. However, in birds (Bilgorajska goose), the diffuse lymphocytes are located both within and around the HEV (Klećkowska-Nawrot, Nowaczyk, et al. 2016; Knop & Knop, 2003(. From the results that mentioned above, the structure of the lower eyelid of black kite enhances ocular immunity than the upper eyelid.