The corneal epithelial surface in the eyes of vertebrates: Environmental and evolutionary influences on structure and function

The smooth optical surface of the cornea is maintained by a tear film, which adheres to a variety of microprojections. These microprojections increase the cell surface area and are thought to improve the movement of oxygen, nutrients, and metabolic products across the outer cell membranes. However, little is known of these structural adaptations in vertebrates inhabiting different environments. This field emission scanning electron microscopic study examined the cell density and surface structure of corneal epithelial cells across 51 representative species of all vertebrate classes from a large range of habitats (aquatic, amphibious, terrestrial, and aerial). In particular, we wished to extend the range of vertebrates to include agnathans and some uniquely Australian species, such as the Australian lungfish (Neoceratodus forsteri), the Australian galah (Eolophus roseicapillus), the Australian koala (Phascolarctos cinereus), and the rat-tailed dunnart (Sminthopsis crassicaudata). Epithelial cell densities ranged from 28,860 +/- 9,214 cells mm(-2) in the flatbead sole Hippoglossoides elassodon (a marine teleost) to 2,126 713 cells mm(-2) in the Australian koala (a terrestrial mammal), which may indicate a reduction in osmotic stress across the corneal surface. A similar reduction in cell density occurred from marine to estuarine to freshwater species. The structure and occurrence of microholes, microplicae, microridges, and microvilli are also described with respect to the demands placed on the cornea in different environments. All species that spend significant periods out of an aquatic environment possess microvilli and/or microplicae. These include all of our species of Mammalia, Aves, Reptilia, Amphibia, and even one species of Teleostei (Australian lungfish). Well-developed microridges occur only in teleosts in high osmolarity environments such as marine or estuarine habitats. Clear interspecific differences in corneal surface structure suggest a degree of adaptive plasticity, in addition to some phylogenetic trends.