For the most part sharks have laterally positioned eyes, ie: the eyes are positioned on the sides of the head. However, some of the more benthic species (eg: orectolobids and squatinids) have more dorsally positioned eyes. When compared with mammals, sharks are considered to have generally small eyes compared to body size, although some species of Lamniforme shark have much larger eyes, including the great white and Mako sharks. In all sharks the two eyes oppose each other which allows for 360◦ visual field, especially in the case of a shark in motion utilising a laterally sinusoidal swimming pattern. Limited eye movements are observed in most species, primarily to compensate for the swimming movements and stabilise the visual field (Harris, 1965). Binocular overlap is small and blind areas exist just in front of the snout and behind the head when the animal is still. The size of these blind areas depends on the shape of the head and the configuration of the eyes, but typically the forward blind area extends less than one body length a head of the rostrum (Carrier et al., 2004).
Fig 1: Cross section through a shark eye showing ocular and retinal anatomy. Tapetum lucidium shown in non-occluded state exposing reflective plates for greater visual sensitivity under scotopic conditions. (Heuter and Gilbert, 1990)
Sharks cannot actually see in colour but instead use contrast in colour to assess their surroundings (Hart et al., 2012). Certainly the importance of vision in the daily lives of sharks finds support in the anatomical and physiological visual adaptations, many of which appear to be correlated with species behaviour and ecology.
Oceanic and deep-sea sharks have the largest eyes amongst sharks and presumably rely more heavily on vision than coastal and benthic species, while variation in the ratio of rod and cone photoreceptors and the spatial resolving power of the eye all appear to be closely related to differences in habitat and lifestyle.
There is evidence that ontogenetic changes in the visual system, such as changes in the spectral transmission properties of the lens, lens shape, focal ratio, visual pigments and spatial resolving power, allow elasmobranchs to adapt to environmental changes imposed by habitat shifts and niche expansion.
Anatomy of a Shark Eye
The outer layer of the shark eye comprises a thick cartilaginous sclera and a gently curving, transparent cornea, the fine structure of which includes sutural fibers that resist corneal swelling and loss of transparency in challenging chemical environments (Tolpin et al. 1969).
Unlike teleosts (bony fish), most sharks have a dynamic iris that can increase the size of the pupil in dim light or decrease it in bright light. The shape of the pupil varies amongst species depending upon their respective feeding strategies. The pupil can be circular (eg. Most deep sea sharks, which have less mobile pupils for more constant, low light conditions), vertical slit (eg. Carcharhinus spp., Negaprion brevirostris), horizontal slit (eg. Sphyrna tiburo), oblique slit (eg. Schyliorhinus canicula, Glinglymostoma cirratum), or crescent-shaped (eg. Many skates and rays) (Carrier et al., 2004). Mobile slit pupils are typically found in active predators with periods of activity in both photopic (bright light) and scotopic (dim light) conditions, such as the Lemon shark, N. brevirostris (Gruber, 1967); a slit pupil that can be closed down to a pinhole is thought to be the best way to achieve the smallest aperture under photopic conditions, because a circular pupil is mechanically constrained from closing to a complete pinhole (Walls, 1942).
Eyelids (Ocular Adnex)
The ocular adnexa (eyelids and adjacent structures to the eye) are well developed in sharks, however the upper and lower eyelids do not move appreciably to cover the entire eye (Gilbert, 1963). Benthic species like the wobbegongs (Orectolobids) have more mobile lids, which serve to protect the eyes whilst burrowing. Some shark species, especially the carcharhinids and sphyrinids, posses a third eyelid, the nictating membrane, which can be extended from the lower nasal corner of the eye to cover the exposed portion of the eye (Gilbert, 1963). The nictating membrane acts to protect the eye during feeding and mating.
The shark cornea is virtually absent underwater due to its similarity in refractive index to the seawater (Heuter, 1991), leaving the crystalline lens to provide the total refractive power of the eye. Shark lenses are typically large, relatively free of optical aberration, and ellipsoidal in shape, although the spiny dogfish, Squalus acanthias, and clearnose skate, Raja eglanteria, have nearly spherical lenses (Sivak, 1991). Some shark lenses contain yellowish pigments that are enzymatically formed oxidation products of tryptophan, similar to lens pigments found in many teleosts and diurnal terrestrial animals. These pigments filter near ultraviolet light, which helps to minimise defocus of multiple wavelengths (Chromatic aberration), enhance contrast sensitivity, and reduce light scatter and glare under conditions of bright sunlight (Zigman, 1991). They may also help to protect the retina from UV damage in shallow benthic or epipelagic species.
At the back of the shark eye behind the retina and in front of the sclera lies the choroid, the only vascularised tissue within the adult shark eye. The shark retina is not vascularised and typically contains no landmarks other than the optic disk (corresponding to a small blind spot in the visual field), which contains no photoreceptors and marks the exit of retinal ganglion cell fibres via the optic nerve from the retina to the CNS. The choroid in nearly all sharks contains a specialised reflective layer known as the tapetum lucidium, which consists of a series of parallel, platelike cells containing guanine crystals (Gilbert, 1963). The function of the tapetum lucidium is to reflect back those photons that have passed through the retina and have not been absorbed by the photoreceptor layer, allowing a second chance for the detection of photons and thereby increasing the sensitivity of the eye in dim light.
Retina and the CNS (Central Nervous System)
The largest impact on our understanding of visual capabilities in sharks came with the eventual finding that practically all sharks have duplex retinas containing both rod and cone photoreceptors (Gruber and Cohen, 1978), beginning with the unequivocal evidence of cones in the lemon shark (N. brevirostris) retina presented by Gruber et al. 1963. Cones subserve photopic and colour vision and are responsible for higher visual acuity; rods subserve scotopic vision and are involved in setting the limits of visual sensitivity in the eye. Prior to Gruber’s work in 1963, sharks were thought to possess all rod retinas, and thus were considered to have poor visual acuity and no capability for colour vision, which we now know to be untrue.
Spatial Topography of the Retina
The spatial topography of retinal cells can, reveal much about the quality of vision in these animals. Although sharks do not have all cone foveas, they do have retinal areas of higher cone and/or ganglion cell density, which indicates regional specialisations for higher visual acuity (Collin, 1999). Higher cone concentrations have been found in the central retina of the nurse shark (G. cirratum) (Gruber, 1965), white spotted bamboo shark (Chiloscyllium plagiosum) (Yew et al. 1984) and the white shark (Carcharodon carcharhias) (Gruber and Cohen, 1985). Franz (1931) was the first to report horizontal streaks of higher ganglion cell density in the small spotted catshark (Scyliorhinus canicula) and the smooth hound (Mustelus mustelus). The horizontal visual streak is an adaptation for more or less two dimensional terrain environments such as the sea bed or the sea surface. Concentric retinal areas are more applicable for imaging a limited spot in the visual field or for operating in complex, three dimensional visual environments, such as reefs or the open water. Both, the cookie cutter shark and the white shark are ambush predators in open water, and both appear to have retinal areas, not streaks (Carrier et al., 2004).
Accommodation is the process by which the vertebrate eye changes optical power to maintain a clear image (focus) on an object as its distance changes. Accommodation acts like a reflex, but can also be consciously controlled, in humans at least. Mammals, birds and reptiles vary the optical power by changing the form of the elastic lens using the ciliary body. Sharks that accommodate do not change the shape of the lens, but instead change the position of the lens by moving it toward the retina (for distant targets) or away from the retina (for near targets). The lens is supported dorsally by suspensory ligaments and ventrally by the pseudocampanule, a papilla with ostensibly contactile function (Sivak and Gilbert, 1976).