The corneal surface of aquatic vertebrates: microstructures with optical and nutritional function?

Abstract

The anterior surface of the mammalian cornea plays an important role in maintaining a smooth optical interface and consequently a sharp retinal image. The smooth surface is produced by a tear film, which adheres to a variety of microprojections, which increase the cell surface area, improve the absorbance of oxygen and nutrients and aid in the movement of metabolic products across the outer cell membrane. However, little is known of the structural adaptations and tear film support provided in other vertebrates from different environments. Using field emission scanning electron microscopy; this study examines the density and surface structure of corneal epithelial cells in representative species of the classes Cephalaspidomorphi, Chondrichthyes, Osteichthyes, Amphibia, Reptilia, Aves and Mammalia, including some Marsupialia. Variations in cell density and the structure and occurrence of microholes, microridges, microplicae and microvilli are described with respect to the demands placed upon the cornea in different aquatic environments such as marine and freshwater. A progressive decrease in epithelial cell density occurs from marine (e.g. 29348 cells mm(-2) in the Dover sole Microstomius pacficus) to estuarine or freshwater (e.g. 5999 cells mm(-2) in the black bream Acanthopagrus butcheri) to terrestrial (e.g. 2126 cells mm(-2) in the Australian koala Phascolarctos cinereus) vertebrates, indicating the reduction in osmotic stress across the corneal surface. The microholes found in the Southern Hemisphere lampreys, namely the pouched lamprey (Geotria australis) and the shorthead lamprey (Mordacia mordax) represent openings for the release of mucus, which may protect the cornea from abrasion during their burrowing phase. Characteristic of marine teleosts, fingerprint-like patterns of corneal microridges are a ubiquitous feature, covering many types of sensory epithelia (including the olfactory epithelium and the oral mucosa). Like microplicae and microvilli, microridges stabilize the tear film to maintain a smooth optical surface and increase the surface area of the epithelium, assisting in diffusion and active transport. The clear interspecific differences in corneal surface structure suggest an adaptive plasticity in the composition and stabilization of the corneal tear film in various aquatic environments.