BIOLOGY OF FISHES FISH/BIOL 311

FORM AND FUNCTION, SENSORY MECHANISMS II: EYES AND VISION; VISUAL PIGMENTS; COLOR VISION General topics:
1. Eye structure 2. Image formation and accommodation 3. Light and dark adaptations 4. Visual pigments and color vision

1. EYE STRUCTURE
The eyes of vertebrates are all built on the same basic plan but those of fishes are characterized by a number of unique structural adaptations that allow them to function properly in an aquatic medium.

retina

lens

iris

posterior chamber

The major features of the eye include an anterior chamber (filled with a liquid, called aqueous humor), an iris, a lens, and a posterior chamber (containing a liquid, called vitreous humor), lined by a multi-layered network of light-sensitive cells, called the retina.

The spherical lens, protruding through the pupil and forming a boundary between the anterior and posterior chambers, is nearly in contact with the cornea, which is essentially a transparent section of the outer layer or scleroid coat of the eyeball. The lens is suspended above and held in place by a suspensory ligament.

scleroid coat choroid layer

suspensory ligament cornea lens

retina

Between the retina and the scleroid coat (sclera) is a highly vascularized choroid layer, which functions primarily to nourish the retina but also serves to absorb stray light or in some species to reflect light back through the retina.

A choroid body or gland, actually a rete mirabile, is prominent in the choroid layer of many teleosts (as well as the bowfin); its structure and function is similar to that of the gas gland of the teleost swimbladder, serving to provide a high partialpressure of oxygen to the retina.

choroid layer

retina nerve fibers choroid body

optic nerve

Fishes have no eyelids (and thus cannot close their eyes) except for the nictitating membranes of certain sharks. The retina consists of an outer pigmented epithelium, the visual cells (rods and cones), a layer of bipolar cells and, closest to the posterior chamber, the ganglion cells and the nerve fibers leading to the optic nerve.

2. IMAGE FORMATION AND

ACCOMMODATION
Fishes live in a medium that has greatly different optical properties than that of air. Depending on the angle of incidence of light, a calm water surface can reflect up to 80% of the light striking it. If the water is rough there is great variation in the transmission of light regardless of the angle of incidence.

The refraction or bending of light rays entering water is such that a fish in water with a perfectly smooth surface views objects above the water through a circle subtended by a 97.2o cone above each eye. Nearly all objects from horizon to horizon appear in the circle, which is surrounded by the reflective under-surface seen beyond the limits of the cone. In rough water the circular window in the surface is broken up and light is transmitted through ever-changing patterns.

Thus, for a fish, vision of objects above the water is highly limited, but vision of underwater objects is a different story. In most fishes, the maximum field of view is achieved by placement of the lens so that it bulges through the opening of the pupil and nearly touches the cornea. The lens can thus gather light practically from an entire hemisphere.

The index of refraction of the cornea is about the same as that of water (1.33), thus it doesnt bend light. Refraction and image formation, therefore, depend almost entirely on the lens. The lens is spherical, with a very high index of refraction (about 1.67).

In contrast to tetrapod eyes, in which accommodation for near and far vision is accomplished by changes in the shape of the lens, the eyes of fishes accommodate by slight anterior and posterior movements of the lens that change the distance between the lens and the retina.

The process by which the distance between lens and retina is modified differs among the major groups of fishes.

Lampreys have a corneal muscle that inserts on the outer transparent covering of the eye. When it contracts, the cornea is flattened, pushing the lens inward, closer to the retina and bringing more distant objects into focus. Lampreys are thus thought of as being myopic or near-sighted.

In elasmobranchs, there are smooth muscle fibers (protractor muscles) located in the anterior part of the choroid layer that pull the lens outward, away from the retina and closer to the cornea; thus accommodation serves to bring near objects into focus. Elasmobranchs are thus thought of as being hyperopic or far-sighted.

A Sharks-eye View: Why are the eyes of hammerheads so widely spaced on their bizarrely shaped heads?
One reason is that it provides a wide range of vision. They see not only directly ahead, but also see up, down, and behind simultaneously. But more importantly, their eye separation gives them great binocular vision and depth perceptiona bonus, especially when pursuing fast-moving prey.

Although hammerheads do have a big blind spot in front of their widely spaced eyes, other senses compensate for this hole in their visual field. Sensors on the their heads help them detect electrical fields emitted by other fishes, and the placement of their nostrils near their eyes could mean that they use enhanced stereo smell to monitor the blind spot.

In teleosts, while the shape of the lens is spherical, or nearly so, the shape of the posterior chamber is such that the retina takes on an ellipsoid. The effect achieved is that relatively distant objects lateral to the fish are in focus but close objects are not. Anteriorly, near objects in the binocular field are in better focus than more distant objects.

Diagram of elliptical eye shape that allows for a large anterior field of vision by a laterally placed eye. Directly in front of the eye is a groove that facilities forward vision.

In teleosts, accommodation to distant vision in the anterior field is accomplished by moving the lens backward by means of a retractor muscle (retractor lentis). Teleosts are thus thought of as being myopic or nearsighted anteriorly, but hyperopic or far-sighted laterally.

anterior

posterior

The ability to accommodate for near and far vision varies considerably among teleosts. In general, fishes that live in wide-open spaces (i.e., most marine teleosts) have welldeveloped retractor lentis muscles and accommodate very well. Most freshwater teleosts, living in habitats where most objects are close-by, have less well-developed muscles and thus have only moderate powers of accommodation.

anterior

posterior

3. LIGHT AND DARK ADAPTATIONS

Regulation of light as it enters, or after it enters, the eye, and adaptation to light or dark, are accomplished in a number of ways. Here are six different approaches: 1. One way to regulate or control the amount of light that enters the eye is to swim toward or away from the source of illumination. 2. Some fishes have pigment in the cornea or lens that acts as a filter to eliminate certain wavelengths. 3. Most elasmobranchs and a few teleosts have contractile irises that control the amount of light that enters the eye.

4. Most rays, many flatfishes, stargazers (family Uranoscopidae), and some catfishes have a pupillary operculum that can expand and cut off most of the light reaching the pupil.

5. Some sharks have nictitating membranes, which are also well developed in many tetrapods, that can be drawn across the eye to reduce excessive illumination.

6. Light and dark adaptation in teleosts is largely accomplished by movements of pigment (melanin) and visual cells (i.e., photoreceptor cells, the rods and cones).

Pigment cells in the outer layer of the retina contain processes through which melanin can move toward or away from the outer parts of the visual cells. Under bright illumination, the eye adapts by movement of melanin toward the visual cells, and by movement of the outer segments of the rods (which are more sensitive to light) into the pigmented area where they are shielded from the light.

In dim light, the pigment is drawn back and the contractile part of the rods pulls them away, exposing them to the light. Movement of the cones (less sensitive to light but allow for color vision) is opposite that of the rods, but the cones are not usually hidden by the pigment. The time required for the shifting of pigment and visual cells in teleosts is considerable: generally, about 30 minutes for light adaptation and an hour or more for dark adaptation.

4. VISUAL PIGMENTS AND COLOR VISION

The distribution of solar radiation that strikes the earth is relatively homogeneous; while the atmosphere does absorb light at the high and low ends of the visual spectrum, its effect is much less significant than that of water.
LIGHT VISIBLE TO HUMANS

Water, in contrast to air, absorbs light rapidly and differentially, with colors at the long or red end of the visual spectrum attenuating rapidly, and those at the short or blue end, penetrating to relatively great depths.
TRANSMISSION OF VISIBLE LIGHT
IN THE OPEN OCEAN IN LAKES AND RIVERS

Thus, unlike terrestrial animals, fishes live in a wide range of visual environments, varying particularly in spectral quality and turbidity.

Pigments, called visual pigments or retinenes, associated with the photoreceptor cells (i.e., rods and cones), are responsible for absorbing light. Different pigments absorb different wavelengths of light; the distribution of pigments present in the retina of a fish determines its sensitivity to various colors.
Visual sensitivity curve for the human eye

Visual sensitivity curves for an intertidal marine fish, Paralabrax clathratus (left), and a marine epipelagic species, Scomber japonicus (right).

Many studies have attempted to relate the visual pigments of different species of fishes to the visual tasks they face in their particular environments. While these studies have revealed an enormous amount of complexity and variation even, in some cases, within individuals of the same species, some general rules appear to hold:

1. Deep-sea species have rod pigments that absorb maximally at relatively short wavelengths (roughly 470 to 490 nm) compared with shallow-water and freshwater species. This is correlated with the predominantly short wavelengths of light (i.e., blue) that penetrate into their environment.

2. Marine fishes living at intermediate depths in coastal waters usually have two cone pigments (apart from the rod pigments) that absorb maximally at around 460 and 540 nm, respectively.

3. Freshwater fishes living near or on the bottom, particularly if they are crepuscular or nocturnal, also often have two cone pigments, absorbing maximally at around 530 and 620 nm. In both cases the long wavelength cones match the spectral quality of the light fairly well.

4. Freshwater fishes living in shallow waters have three cone pigments, two of them similar to those of the deeper-living forms, but with a bluesensitive cone in addition, absorbing maximally at around 430 nm.

The presence of three as opposed to two cone types, covering a wider range of the spectrum, presumably correlates with the wider spectrum of light available to them.

5. Fishes inhabiting very shallow fresh waters or marine tide pools also usually have three cone pigments, but the green and red cone pigments are shifted towards short wavelengths and are comparable in their spectral positions to the cones of terrestrial animals.

The light environment in very shallow water is obviously similar to that of terrestrial animals, because the filtering effect of the water will be small.

6. A number of species have cones sensitive in the ultraviolet range, with an absorption maximum that lies around 355360 nm.

Ultraviolet light is heavily absorbed by water, present at any intensity only in the surface layers, and in some species ultraviolet sensitivity correlates with living near the surface. It is not known what use fish make of their ultraviolet sensitivity.

7. In addition to the blue spectrum, some deep-sea fishes see in the red spectrum, i.e., at wavelengths greater than 570 nm.

This capability is extremely rare, found as far as we know only in some deep-sea fishes of the family Stomiidae. For example, Photostomias patrox, just recently described as new to science by former SAFS graduate student Chris Kenaley.

Heres another member of the deep-sea family Stomiidae, Malacosteus niger, showing the probable function of red-light productionilluminating prey that is otherwise invisible to organisms lacking long-wave visual pigments.

Malacosteus niger in the process of devouring prey.