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.