Vision (marine mammals)

The vision of marine mammals has a number of specific features associated with its ability to function in both water and air. Although many marine mammals (cetaceans, sirenians) spend their entire life in water, their aerial breathing confines them to a near-surface layer of water. Other marine mammals (pinnipeds, sea otters) spend a significant part of their life on land. As a result, the organization of their visual system fits requirements of both these different media. Although some aspects of organization of the visual system of marine mammals still remain unstudied, many features of their vision are known already.

I. Visual Abilities of Marine Mammals

A, Cetaceans

It was long believed that dolphins—animals with excellent hearing and echolocation—have a poorly developed visual system playing a minor role in their life. However, observations of the visual activity of dolphins have demonstrated the opposite. The ability to catch fish in air, to perform precisely aimed jumps to reach targets above the water, and to recognize their trainers al] show that vision in dolphins is well developed. In conditions of captivity, dolphins decrease their use of echolocation and, as their interest in events above the water increases, vision takes on a leading role.

Reviews of Madsen and Herman (1980) and Mobley and Helweg (1990) summarize observations of dolphins in captivity and experimental studies that provide a basis for regarding the vision of dolphins as playing an important role in various aspects of their life: in social interactions, in discrimination between individuals and species based on their colors and individual marks, in the search and discrimination of prey, in orientation, in reproductive activity, and in defense. Only vision provides the ability for rapid and precise assessment of distances to objects in air where echolocation does not operate.

Apart from numerous observations, good visual abilities of cetaceans were demonstrated in behavioral experiments for assessing their visual acuity. Precise behavioral measurements performed by Herman and colleagues (see Madsen and Herman, 1980) on the bottlenose dolphin (Tursiops truncatus) resulted in an estimate of underwater visual acuity of 8.2 arc min (at the best distance of 1 m) and aerial visual acuity of 12.5 arc min (at distances of 2.5 m and longer). In general, estimates of visual acuity in dolphins varied from 8 to 27 arc min in water and from 12 to 18 arc min in air.

Studies of color vision in cetaceans are very few in number. Only one cone type was found in the bottlenose dolphin, widi the best sensitivity at 525 nm; rods are best sensitive to 488 nm. These sensitivity peaks are considerably blue-shifted as compared to those of many terrestrial mammals (Jacobs, 1993). Therefore, the dolphin lacks the common dichromatic vision typical of many terrestrial mammals, which is based on two cone types with different chromatic sensitivity. If color vision is present in dolphins (basing on comparison of signals from rods and cones), it is poorly developed and limited to a blue-green region of the spectrum.

In all cetaceans, the eyes are positioned laterally, thus providing a visual field as wide as 120-130° and panoramic vision. Although positioned laterally, the eyes are directed somewhat forward and downward (ventronasally). On viewing visual objects in air, the dolphin eyes can move forward by 10-15 mm so that the visual fields of the two eyes overlap by 20-30° in the frontal sector, giving a basis for binocular vision. However, uncrossed optic fibers have not yet been demonstrated in dolphins. Therefore, the existence of true binocular (stereoscopis) vision (based on interaction of crossed and uncrossed optic fibers) in dolphins still remains under question.

Dolphins are equally capable of the perception of complex configurations of objects using both vision and echolocation. Besides, there is also a possibility of intermodal transfer between these two modalities: objects known for a dolphin only by visual appearance can be discriminated and recognized by echolocation, and vice versa. The intermodal transfer is equally successful when visual experience is used for echolocation discrimination and when echolocation experience is used for visual discrimination.

Even in riverine cetaceans inhabiting turbid and low-transparent water (the Amazon river dolphin, Inia geoffrensis, the tucuxi, Sotalia fhwiatilis), the visual system does not exhibit a significant regression. The only exception is the Indian river dolphin, Platanista gangetica, in which the visual system is reduced markedly.

B. Pinnipeds

Because pinnipeds spend their life partially in water and partially on land, they use both underwater and aerial vision. On land, vision plays an important role during the reproductive period, during birth and feeding of pups, and for maintaining intrapopulation relationships, as well as for orientation. In water, vision is used for prey detection and recognition, for avoiding predators, and for spatial orientation during migrations.

Because of a great diversity of pinniped species in terms of systematic position and ecology, the role of vision diverges widely as well. Walruses (Odobenus rosmarus) rely mainly on their vibrissa] sensitivity to identify objects during benthic foraging. Other pinnipeds also have a well-developed vibrissa] apparatus; however, in aquatic conditions, most seals use both visual and tactile modalities to search for food. Experiments demonstrated that seals are able to distinguish rather small objects visually, to recognize the shape of figures, and to perform a complex analysis of visual images. Data summarized by Fobes and Smock (1981) showed that both otariids and phocids are capable of discriminating objects differing in size from 9 to 24%.

Most pinnipeds (both otariids and phocids) have maximum spectra] sensitivity within a range of 496-500 nm. An exception is the southern elephant seal (Mirounga leonina), which is sensitive to a shorter wavelength (486 nm).

A possibility of limited color discrimination in a few pinniped species (Pagophilus groenlandicus, Phoca larga, Arctocephalus pusillus, A. australis) is indicated by their capability to discriminate blue and green objects from gray ones, although they cannot discriminate red and gray objects. The best rod sensitivity in the harbor seal (Phoca vitulina) was found at 496 nm and cone sensitivity at 510 nm; i.e., similar to dolphins, the spectral sensitivity is blue-shifted as compared to terrestrial mammals. No indication was obtained of more than one cone type in pinnipeds.

Measurements of visual acuity based on the use of grids as test stimuli have demonstrated that visual acuity in both water and air is 5-8 arc min in a few otariid species: Zalophus californianus, Eumetopias jubatus, Arctocephalus pusillus, and A. australis.

C. Other Marine Mammals

1. Sirenians There has been no detailed investigation of visual capabilities in sirenians. A few observations summarized by Piggins et al. (1983) showed that the Amazon manatee (Trichechus inunguis) is capable of visually driven behavior, particularly visual tracking of underwater objects. A capability of the Caribbean manatee, Trichechus manatus, for dichromatic (blue-green) color vision has been shown. It remains unknown whether the manatee has an ability of good aerial vision.

2. Sea Otters Very little is known of the visual abilities of sea otters (Enlujdra lutris). Inhabiting the coastal zone and feeding underwater, sea otters need to have good vision in both air and water. Observations showed that they actively use vision, and experiments have shown their capability to discriminate objects of different sizes. However, quantitative behavioral measurements of their visual abilities are absent.

II. Eye Anatomy and Optics

A. Cetaceans

Ocular anatomy in cetaceans is markedly different from that in terrestrial mammals by being adjusted to optical properties of water and to a number of other factors: possibility of eye damage because of high density of water and presence of suspended particles, low temperature and low illumination deep in water, significant light scatter, and so on. Characteristic examples of eye structure in cetaceans are shown in Fig. 1. Remarkable features are a thick sclera (especially so in whales, Fig. IB), a thickened cornea, a highly developed vascular network forming a typical vascular rete mirabilia, which fills a significant part of the orbit behind the eyeball, and massive ocular muscles. All of these structures take part in protecting the eye from underwater cooling and mechanical damage.

While in terrestrial mammals the eyeball is almost spherical, in cetaceans its anterior part is flattened so that the anterior chamber is small and the eyecup is of almost a hemispherical shape. More precisely, the eyecup shape approximates a segment of a sphere of about 150° of arc (Figs. 1A and IB), and its nasotemporal diameter slightly exceeds the dorsoventral one.

In terrestrial mammals, the convex outer surface of the cornea is the major refractive element of the eye because it separates media with different refractive indices: air with a refractive index of about 1 and the corneal tissue with a refractive index of more than 1.35. However, the refractive index of water is 1.33-1.34, which is very’ close to that of the cornea and the intraocular media. As a result, the corneal surface plays very little part in underwater light refraction. Therefore, in cetaceans, light refraction and focusing of an image on the retina are almost entirely performed by the lens. This is why the lens in cetaceans is almost spherical or slightly elliptical. The large curvature of the lens surface provides a sufficiently high refractive power of the lens and well-focused images on the retina, despite very weak refractive power of the corneal surface in water. These optics are similar to those in fish, which is not surprising given that in both cases the eye is adjusted to optical properties of the same medium.

Figure 1 Schematic presentation of eye anatomy and optics in some cetaceans: (A) the common bottlenose dolphin, (B) the gray whale (Eschrichtius robustus), and (C) the Amazon river dolphin. Co, cornea; L, lens; Ir, iris; O, opercidum; S, sclera; Ch, choroid; R, retina; ON, optic nerve; OD, optic disc; VB, vitreous body. Arrows 1 and 2 delimit a part of the eyecup, which can be approximated by a spherical segment of about 150°. Arrotvs 3 and 4 show directions of light rays passing through the nasal and temporal holes of the pupil and through the lens center to the high-resolution parts of the retina.

A strongly convex (spherical) lens consisting of homogeneous material has a very strong spherical aberration. The cetacean lens is free of this disadvantage due to a heterogeneous structure: outer layers have a lower refractive index than the inner core.

In the cetacean eye. the spherical lens is located in such a way that its center almost coincides with the center of the spherical segment of the eyecup, so light rays coming from any direction are focused almost identically on the retina. This is significantly different from the case in terrestrial mammals, which provides the best focusing on the eye axis.

In terrestrial mammal eyes, accommodation (refraction adjustment to the distance to the object) is performed by a change in the shape of the lens due to contraction and relaxation of ciliary muscles. In cetaceans, spherical lens shape and center-symmetric optics of the eye led to loss of this accommodatory mechanism. The ciliary muscles are poorly developed in dolphins and are absent in most whales, suggesting that accommodation cannot be achieved by changing the lens shape. It has been suggested that accommodation in cetaceans is performed by another mechanism, namely by axial displacement of the lens due to changes in intraocular pressure. Intraocular pressure can change because of contraction of the retractor/protractor muscles, which produce axial displacements of the eye in the orbit. When the eye is pulled back into the orbit, intraocular pressure increases, thus shifting the lens forward: when the eye is moved forward, the pressure decreases, shifting the lens backward.

The cornea in cetaceans is thicker than in many terrestrial mammals, and this thickness is not uniform: the cornea is thinner in the center and thicker in the periphery. Although major refraction in the cetacean eye is performed by the lens, the refractive role of the cornea is not negligible. Its outer surface is of lower curvature than the inner one; i.e.. the cornea has a shape of a divergent lens. Under water, this lens makes a minor contribution to the total refraction power, as the media on both sides of the cornea (water outside and the anterior chamber liquid inside) have refractive indices rather close to that of the cornea. However, some difference between the refractive indices of water (1.33) and the cornea (from 1.37 in the central part to 1.53 in the periphery) does exist. Thus, the cornea acts a weak but nonetheless divergent lens. The total refraction of the cornea and lens makes the cetacean eye well emmetropic within a range of ± 1 diopters under water.

Adaptation to underwater vision also affects the cetacean iris and pupil. Cetacean vision functions in conditions of wide and rapid changes of illumination when the animal dives from the well-illuminated water surface into the depths where illumination is very low. This requires the pupil to react in a wide range of illuminations and to have a wide range of sizes. The cetacean pupil is of an unusual shape. The upper part of the iris has a characteristic protuberance, the operculum. At low illumination, the operculum is contracted (raised), so the pupil, similarly to other mammals, is of a round or slightly oval shape; its horizontal diameter in dolphins is of about 10 mm (Fig. 2A). With illumination increased, the operculum advances downward, turning the pupil into a U-shaped slit (Fig. 2B). At high illumination, the operculum advances so far diat the slit becomes closed, leaving only two narrow holes in the temporal and nasal parts of the iris (Fig. 2C). This pupil shape is characteristic for many dolphins, including the bottlenose dolphin, harbor porpoise (Phocoena phocoena). common dolphins (Delphinus spp.), tucuxi, and also for a number of whales, although in some whales the operculum is small. A known exception is die Amazon river dolphin, which has a round pupil even when it is constricted.

The cetacean eye is well emmetropic in water; however, in air refraction on the outer convex corneal surface adds to the lens refraction. The difference of refractive indices of air and the cornea results in significant refractive power of the central most convex part of the corneal surface: about 20 diopters. The addition of this refraction to the emmetropic lens refraction should make the cetacean eye catastrophically myopic (near-seeing) in air. Nonetheless, dolphins have good visual acuity in both water and air.

The solution of the problem is in the presence of flattened (low-curvature) regions of the cornea. A flat corneal surface does not produced additional refraction in air. Even if the surface is not truly flat but a little convex, its refractive power becomes low enough and may be compensated by some additional mechanisms. Keratoscopis studies in common bottlenose dolphins showed a “spoon” shape of the cornea with lower curvature in its nasal and temporal regions.

Aerial myopia can be partially compensated by accommodatory displacements of the lens. For aerial vision, the dolphin eve moves forward, thus producing a decrease of intraocular pressure; this results in shifting the lens backward and reduced myopia. Additionally, reduction of intraocular pressure decreases the curvature of the cornea. Under water, the eye is retracted into the orbit, which results in increased intraocular pressure and a shift of the lens forward to a position providing underwater emmetropia.

An additional mechanism for the correction of aerial myopia is pupil constriction. Above water, high illumination results in strong pupil constriction; the latter corrects all errors of refraction, including aerial myopia, and provides a fairly good depth of field.

Figure 2 Shape of the pupil in the common bottlenose dolphin at various levels of illumination: (A) loiv illumination, nonconstricted oval pupil; (B) moderate illumination, partially constricted U-shaped pupil: and (C) high illumination, strongly constricted pupil reduced to two pinholes.

Another adaptation of the cetacean eye to low underwater illumination is the well-developed reflective layer, the tapetum lucidum. It lies behind the retinal pigment epithelium within the choroid. In cetaceans, the tapetum is formed with extracellular collagen fibrils {tapetum fibrosum). Multiple reflection of light from 50 to 70 layers of fibrils results in significant light reflection back to the retina, thus increasing visual sensitivity in scotopic conditions.

The tapetum is present in all cetaceans. In most investigated cetaceans, particularly in mysticete whales, it covers all of the fundus (although it varies in coloration), or at least it covers a large dorsal part of the fundus. Complete coverage of the fundus by the tapetum is unique among vertebrates: in terrestrial mammals, the tapetum usually does not extend lower than the horizontal equator of the eyecup.

B. Pinnipeds

In all pinnipeds (except walruses), bodi the absolute and the relative sizes of the eyeball are large. The eye structure in pinnipeds (Fig. 3A), despite significant differences from cetaceans, has some common features arising from adaptation to underwater vision (Jamieson and Fisher, 1972). In particular, a characteristic feature is an almost spherical or slightly elliptical lens. Although the eyeball does not appear as shortened in the axial direction, a major part of the eyecup has a shape close to a hemisphere so a significant part of the retina is almost constantly distant from the lens center. Thus, the eye optics, like in cetaceans, is almost centrally symmetrical. The difference between the eyeball shape in cetaceans and pinnipeds (shorter axial length in cetaceans and longer in pinnipeds) is mainly due to the larger size of the anterior chamber in pinnipeds.

The iris in pinnipeds is very muscular and heavily vascularized. The dilator is well developed. All pinnipeds have a pupil, which being constricted becomes pear-shaped, except for a diagonal pupil in the bearded seal, Erignathus barbatus. Pupil size can change over a very wide range; at bright illumination, it constricts to a very small hole. The ciliary muscle in pinnipeds is well developed, although accommodation is either absent or very weak.

Unlike cetaceans, the central part of the cornea has a clearly delimited region (6-10 mm in diameter) of almost a flat surface. It is located near the center of the cornea, slightly shifted to the nasal direction (FC region in Fig. 3A). Such a flat region of the cornea was found in a number of both otariids and phocids and was demonstrated by precise measurements on the Californian sea lion (Zalophm californianus). The flat region of the cornea serves as an emmetropic “window” in which refraction remains almost equal in both water and air. In another pinniped, the hooded seal (Cystophora cristata), the flattened part of the cornea does not look like a delimited region but arises because of low curvature of the cornea of the extremely large eyeball.

The existence of a flat region in the central part of the cornea indicates a very specific principle of eye construction in pin nipeds. Indeed, the convex shape of the cornea in most animals is a consequence of excessive intraocular pressure, which is necessary for maintaining the shape and size of the eyeball. Direct data on intraocular pressure in pinnipeds are absent, but their flat cornea suggests that this pressure is very low, perhaps about zero. Anatomical observations on the northern fur seal (Cal-lorhinus ursinus) showed that its vitreous body is of a rigid radier than a gelatinous consistency, thus taking a part in maintenance of the eyeball shape and dimensions. This way of maintaining the eye shape is evidently used in a number of pinniped species.

Figure 3 Schematic presentation of eye anatomy and optics in some representatives of pinnipeds, sirenians, and otters: (A) the northern fur seal, (B) the manatee, and (C) the sea otter. Co, cornea; FC, flattened region of the cornea; L, lens; Ir, Iris; S, sclera; Ch, choroid; R, retina; ON, optic nerve; OD, optic disc; P, lens protuberance; VB, vitreous body.

The pinniped tapetum is one of the best developed among both terrestrial and aquatic mammals. Contrary to the tapetum fibrosum in cetacean, the tapetum in pinnipeds is formed with intracellular reflective rodlets (tapetum cellulosum). It consists of a large number (20-30 or more) of cell layers and covers all of the fundus.

C. Other Marine Mammals

1. Sirenians Among other marine mammals, the eye anatomy of the manatees (Trichechus manatus and T. inunguis) is of interest as an example of the order Sirenia, which, apart of cetaceans, is the only group of completely aquatic mammals.

Both in T. manatus and T. inunguis the eye is rather small (13-19 111111 diameter) and is set deeply within the ocular fascia. Its general morphology resembles more that of terrestrial mammals than the cetacean eye (Fig. 3B). The eyeball is almost spherical (the axial length differs little from the equatorial diameter), the anterior chamber is shallow, and the lens is set forward and is not truly spherical: its axial dimension is markedly shorter than the diameter. The sclera is rather thin. Thus, despite the completely aquatic mode of life of the manatee, its eye anatomy exhibits a number of conservative features (Piggins et al, 1983). Underwater, the eye is almost emmetropic or slightly hyperopic, but in air it is strongly myopic. It remains unknown whether the manatee has some mechanism to compensate aerial myopia; thus, its capability to aerial vision remain unknown.

2. Sea Otters To a large extent, the eyeball of the sea otter (Enhydra hitris) is similar to those of terrestrial mammals (Fig. 3C): it is almost spherical, the axial length is only a little shorter than the diameter. Contrary to spherical lenses of cetaceans and pinnipeds, the lens of the sea otter is lenticular. However, the front surface of the lens has a protuberance of increased curvature. A characteristic feature of the eye anatomy is that the iris is fastened to the frontal lens surface. Therefore, contraction of iris muscles influences the curvature of the frontal lens surface. This mechanism is capable of providing an accommodation range of up to 60 diopters, thus compensating for the appearance of refraction at the corneal surface in air and its disappearance in water. This accommodation mechanism in the sea otter eye is able to preserve emmetropia in both air and water.

III. Eye Movements

All dolphins and whales have mobile eyes. However, measurements in the bottlenose dolphin indicate that eye mobility is less than in humans, and eye movements are slower.

Oculomotor muscles are well developed in dolphins and whales; an exception is the Indian river dolphin (Platanista gangetica), which has reduced eyes and no oculomotor muscles. Other cetaceans have a complete set of muscles known in mammals: four straight and two oblique muscles. These muscles allow eye movements in both the horizontal and the vertical directions. In addition, unlike terrestrial mammals, cetaceans have retractor/protractor muscles (m. retractor bulbi and m. protractor bulbi), which produce axial (in/out) movements of the eye in the orbit. The botdenose dolphin is capable of moving its eye forward 10-15 mm and pulling it back. As a rule, forward eye movements (protraction) appear when the dolphin examines an object in air visually. These eye movements may be used for the binocular examination of objects. As mentioned earlier, the eye protraction in air can also provide accommodation to avoid aerial myopia.

Another intriguing factor of oculomotor activity in dolphins is the ability to move the left and right eyes independently. Quantitative measurements in dolphins have shown that the correlation of movements of the left and right eyes is very low; i.e., independent eye movements in dolphins are a rule rather than exception.

In addition to independent eye movements, cetaceans have rather independent pupil reflexes of the two eyes. Moreover, eyelids of the left and right eyes can also function independently so one eye can be open while the other is closed. Such observations were made during sleep in dolphins, although similar behavior is also possible in wakefulness: dolphins can swim for long periods with one eye open and the other one closed, with the left and right eye alternating.

As to pinnipeds and sea otters, there is no significant difference from terrestrial mammals in their oculomotor muscle anatomy and the character of eye movements.

IV. The Retina and Optic Nerve

A. Features of the Retina in Cetaceans

The histological structure of the retina has been investigated in a number of cetacean species: the common bottlenose dolphin, short-beaked common dolphin (Delphinus delphis), Dall’s porpoise (Phocoenoides dalli), dwarf sperm whale (Kogia sima), Amazon river dolphin, fin whale (Balaenoptera phtjsalus), and common minke whale (B. acutorostrata). All of these studies have shown that the laminal structure of the cetacean retina is basically similar to diat in terrestrial mammals. The retina consists of typical layers as follows (Fig. 4). The receptor layer (the nearest to the pigment epithelium) is composed of densely packed outer segments of photoreceptors. The outer nuclear layer is composed of receptor pericaria arranged in a multilevel manner. The outer plexiform layer contains cell processes establishing connections between receptors and first-order neurons, bipolar cells. The inner nuclear layer is composed mostly of pericaria of bipolar cells; in addition, this layer contains horizontal and amacrine cells, which establish horizontal connections within the outer and the inner plexiform layers. The inner plexiform layer contains processes establishing connections between bipolar and ganglion cells. The ganglion layer contains ganglion cells sending their axons to the optic nerve. Finally, the nerve fiber layer (nearest to the vitreous body) contains optic fibers (axons of ganglion cells), which spread along the inner/retinal surface until they reach the optic disk and enter the optic nerve. This laminar structure of the retina is fully developed in all cetaceans. Even in the Indian river dolphin with strongly reduced eyes, the retina contains all the layers. Being basically similar in cetaceans and terrestrial mammals, the retina has a number of specific features in cetaceans. It is markedly thicker than in terrestrial mammals, ranging from 370 to 425 p,m (in terrestrial mammals, the retina is 110-240 |xm thick).

Figure 4 Microphotographs of a transverse section of the retina of a Dall’s porpoise. PE, pigment epithelium; RL, receptor layer; ONL, outer nuclear layer; OPL, outer plexiform layer; 1NL, inner nuclear layer; IPL, inner plexiform layer; GL, ganglion layer; NFL, nerve fiber layer.

The most detailed description of the retina is available for the common bottlenose dolphin (Dial, 1977; Dawson, 1980). Its retinal receptor layer consists predominantly of rods (receptors for achromatic vision). The question of the existence of cones (chromatic-vision receptors) in cetaceans is still debatable; if cones exist, they are few in number. This corresponds to behavioral data showing poor color vision in dolphins (see Section I,A). As to amacrine, bipolar, and horizontal cells in the cetacean retina, they are generally similar to those in terrestrial mammals.

A marked difference from terrestrial mammals is in the inner plexiform layer and the ganglion layer of the cetacean retina. The ganglion layer looks like a single row of large, sparsely distributed neurons separated by large intercellular spaces. These neurons have large cell bodies with a clearly defined cell membrane, a large amount of cytoplasm, a well-visible nucleus up to 15 p,m in diameter, and a clearly defined nucleolus 4-5 p,m in diameter. Cell bodies contain clearly visible, well-stained Nissl granules.

A remarkable feature of the cetacean retina is the large size of ganglion cells, particularly the presence of giant ganglion cells. Bodies of such cells reach 75-80 |xm, sometimes more. Giant ganglion cells were described in a number of odontocete species and in a few mysticete whales. In some dolphins, however, retinal ganglion cells do not reach giant sizes: in the Amazon river dolphin and the Indian river dolphin they do not exceed 40^12 and 20 jjuii, respectively. However, even these cells are large as compared to those in many other mammals. The smallest ganglion cells in cetaceans are as large as 10 p,m.

Figures 5A and 5B present ganglion cell size distributions in the retina of the common bottlenose dolphin. The histograms represent samples in different parts of the retina: with high and low concentration of ganglion cells. Despite some difference between the samples (in the area of high cell concentration, cells are a little smaller than in the area of low concentration), bodi samples demonstrate large cell sizes: the most common size is 20-35 |xm, but cells as large as 50-60 |xm are also present; there are no cells smaller than 10 |xm.

Large cells are not characteristic of all levels of die visual system in cetaceans (the lateral geniculate body, visual cortex); they are typical only in the retina. The largest pyramidal cells in the visual area of the dolphin cerebral cortex are not more than 20-30 ixni. In other parts of the dolphin brain, cells do not exceed 20-45 |xm either. There is presently no satisfactory explanation why ganglion cells in die cetacean retina are so large. One possible explanation is diat large ganglion cells have thick axons with a high velocity of conduction; in a large body, it may be helpful for die fast transmission of signals. However, large terrestrial mammals (e.g., the bull or elephant) have ganglion cells no larger dian 25-30 |xm.

Figure 5 Histograms showing size distributions of ganglion cells in the retina of cetaceans and pinnipeds. Abscissa axis, cell size: ordinate axis, number of cells of the present size. (A and B) Data from a common bottlenose dolphin; samples from areas of high (A) and low (B) cell densities. (C and D) The same for a northern fur seal.

Apart from large cell sizes, a characteristic feature of the retinal ganglion layer in cetaceans is low cell density. The large neurons are separated by large intercellular spaces.

The question of separation of retinal ganglion cells into different morphological types has not been solved for cetaceans. Large-size ganglion cells in cetaceans resemble large Y neurons in the visual system of terrestrial mammals, as opposed to smaller X neurons. However, Y neurons in terrestrial mammals constitute no more than 1% of ganglion cells, whereas in cetaceans, large ganglion cells predominate.

B. Optic Nerve Structure in Cetaceans

Retinal ganglion cells send their axons into the optic nerve. Consistent with the large sizes of ganglion cell bodies, the axon diameters in cetaceans are also greater than in terrestrial mammals. In a variety of dolphin species, a significant proportion of optic fibers exceed 15 p,m in diameter. For comparison, the maximum fiber diameter in cats and monkeys is no more than 8 |o.m. The only exception is the Chinese river dolphin, Lipotes vexillifer, which has thin optic fibers, although its retina contains ganglion cells as large as 75 p-m.

The low density of ganglion cells in the retina of cetaceans corresponds to the low density of fibers in the optic nerve. In cross sections of the optic nerve of dolphins, the density of fibers is less than 50,000/mm”, whereas in monkeys it exceeds 220,000/mm2. Thus, although the optic nerve in cetaceans is of a larger diameter, the total number ol optic fibers does not exceed that in many terrestrial mammals. More than 50% of the cross section area of the cetacean optic nerve is occupied by intercellular space (as opposed to 12-20% in terrestrial mammals), not by glia.

The total number of optic fibers varies among cetacean species. The smallest number of fibers (14,000-16,000) was found in the Indian river dolphin, Platanista gangetica, and the Amazon river dolphin, Inia geoffrensis; the number of optic fibers in the Chinese river dolphin, Lipotes vexillifer, is a little higher, more than 20,000. In the common bottlenose dolphin, the number of optic fibers is 150,000-180,000. Other odontocetes have an optic fiber number similar to that in the bottlenose dolphin. In mysticetes, the number of optic fibers is within a range of 250,000-420,000.

C. Features of the Retina in Pinnipeds

In general, the retinal structure in pinnipeds is the same as in terrestrial mammals. All layers are present in the pinniped retina, although there are a number of specific features, mainly of the inner nuclear and ganglion layers (Jamison and Fisher, 1972).

The inner nuclear layer in pinnipeds does not have clear margins, in contrast to terrestrial mammals, where this layer is strictly ordered. There are large horizontal cells with very long processes within this layer. The giant horizontal cells are located irregularly among bipolar and amacrine cells, which are also distributed chaotically. Bipolar cells are located mostly in the outer part of the inner nuclear layer while large amacrine cells are located close to the inner plexiform layer.

The ganglion layer in pinnipeds consists of a single row of ganglion cells separated by wide intercellular distances. Ganglion cells have large pericaria, a large amount of Nissl substance in the cytoplasm and long dendrites. Most of these cells are of intermediate size (10-30 p-m), although large cells (up to 50 p,m) are also encountered (Figs. 5C and 5D). These sizes are smaller than in cetaceans, although larger than in terrestrial mammals.

All pinnipeds have a predominately rod retina. However, light and electron microscopy has shown the presence of cones in the harbor seal and harp seal, although photoreceptors of this type are not numerous. The existence of some amount of cones corresponds to behavioral data showing a limited capability of color discrimination in pinnipeds (see Section I,B).

D. The Retina of Other Marine Mammals

1. Sirenians The retina of the manatees also features the common laminar organization. Receptors are presented mostly by rods; cones are less numerous. Among specific features, the large size of the ganglion cells can be mentioned: up to 60 p-m, mostly 15-30 p,m, and not less than 10 p.in. Thus, the large size of ganglion cells seems to be a common feature of different groups of marine mammals.

2. Sea Otters In the sea otter, the retina has many features similar to those in terrestrial rather than in aquatic mammals. The majority of ganglion cells are not of large size: 7 to 30 p,m, mostly 11-15 p,m. They can be subdivided into three size groups: large, medium, and small. The retina of the sea otter contains a large number of small amarcine and neuroglial cells.

V. Retinal Topography and Visual Field Organization

A. Cetaceans

Ganglion cells are distributed nonuniformly in the mammalian retina: ganglion cell density (number of cells per area unit) is high in some areas and much lower in the remainder of the retina. Regions of ganglion cell concentration (high density) provide the most detailed analysis of visual images. Characteristics of retinal topography in a variety of mammals are presented in a review by Hughes (1977).

In terrestrial mammals, there are two main types of organization of a region with high cell density. In mammals with frontal vision, highest density is in the fovea or area centralis located in the center of the visual field. This retinal area is little vascularized to avoid its shadowing by blood vessels. In mammals with laterally located eyes, the region of high cell density is shaped as a narrow horizontal strip, the visual streak. All terrestrial mammals studies up until now have only one, if any, region of highest ganglion cell density.

The cetacean retina does not have avascular areas, indicating the presence of fovea or area centralis. Therefore, visual examination of the eye fundus is not capable of revealing such regions. Data on the topographv of ganglion cell distribution in the cetacean retina were obtained using retinal whole mounts. Whole mounts are preparation of a total retina flattened on a slide, ganglion layer upward, and stained appropriately. Retinal whole mounts allow one to count ganglion cells systematically across all of the retina surface, thus constructing a topographic map of ganglion cell distribution. Studies of retinal whole mounts have shown that different regions of the cetacean retina have a very different density of ganglion cells (Fig. 6). Beginning from the pioneering studies of Dral (1977), studies of cetacean retinal whole mounts were performed in a number of dolphin species, particularly the common dolphin, common bottlenose dolphin, harbor porpoise, Dall’s porpoise, and Pacific white-sided dolphin (Lagenorhynchus obliquidens) (see review by Mass, 1997).

The most characteristic feature of these species is that, unlike terrestrial mammals, all of these marine dolphins do not have a single area of high ganglion cell density but two such areas. They are located near the horizontal diameter of the retina, one in the nasal and the other in the temporal sector (Fig. 7A). In the bottlenose dolphin, both of these areas are located at a distance of 15-16 mm from the optic disk, which corresponds to 50-55° of the visual field. Ganglion cell density in each of these areas reaches 700-800 cells/mm2, which corresponds to 40-50 cells per squared degree of the visual field (cells/deg2). The two high-density areas are connected by an elongated zone of increased, although somewhat lower, cell density, which runs below the optic disk; this zone looks like a visual streak.

In other dolphin species, the retinal topography is basically similar to that described earlier: there are two areas of high ganglion cell density. Even at low cell density in some cetaceans inhabiting turbid and low-transparent water (e.g., the tucuxi), the retinal topography looks the same (Fig. 7B). However, some quantitative differences do exist. In the bottlenose dolphin, the ganglion cell density is almost equal in the two areas, the nasal and the temporal areas, whereas in the harbor porpoise, the cell density in the temporal area (i.e., the region serving the frontal visual field) is higher than in the nasal region: 28 and 20 cells/deg2, respectively.

The retinal topography of ganglion cells was studied in two mysticete species: the gray whale, Eschrichtius robustus, and common minke whale (Balaenoptera acutorostrata). Both of them also have ganglion cell distributions with two area of high cell density in the nasal and temporal sectors (Fig. 7C). Again, the cell density in the temporal area is higher than in the nasal one: 28 and 21 cells/deg2 in the gray whale.

The significance of the two areas of high ganglion cell density (i.e., of high retinal resolution) is probably associated with the cetaceans capability of good vision both above and under water, in particular, with preventing aerial miopia. Indeed, the high-resolution areas are located just opposite the two small pupil holes formed when the pupil is constricted in air (see Fig. 1A). Because of the centrally symmetric optics of the cetacean eye, light falls onto each of these areas through the opposite hole of the pupil. The areas of the cornea with minimal curvature are located across from these narrow pupil holes. Both the pinhole pupils and the low cornea curvature are devices to prevent aerial miopia. Thus, images are projected onto the high-resolution areas of the retina with minimal distortions.

The two high-resolution retinal areas in cetaceans may be used differently for underwater and aerial vision (see Mass, 1997). When a dolphin looks at an underwater object, it takes a position lateral to the object; i.e., the object is placed into the posterolateral part of the visual field, which projects onto the nasal high-resolution area of the retina. On the contrary, when a dolphin looks at an object above water, it places the object into the ventronasal part of the visual field, which projects onto the temporal high-resolution area of the retina (Fig. 8). Of course, the temporal high-resolution area of the retina also participates in underwater vision. This area serves the frontal part of the visual field, which is very important for forward-moving animals. The existence of two high-resolution areas of the retina can also compensate for the limited head mobility in many cetaceans. At low head mobility, even at high mobility of the eyes, a single high-resolution area allows the animal to inspect only a limited part of the surrounding space, whereas two such areas can provide almost panoramic vision.

Figure 6 Microphotographs of the ganglion layer in a retinal whole mount of a bottlenose dolphin: (A) an area of high cell density and (B) an area of loty cell density.

Figure 7 Topographic distribution of ganglion cell density in the retina of some cetaceans: (A) the common bottlenose dolphin, (B) the tucuxi dolphin, (C) the gray whale, and (D) the Amazon river dolphin. Cell density is expressed as number of cells per squared degree of the visual field and is shown by various shadowing, according to the scales. Concentric circles show angular coordinates on a retinal hemisphere centered on the lens. D, V, N, T, dorsal, ventral, nasal, and temporal poles of the retina, respectively.

Figure 8 Characteristic positions of the dolphin body relative to visually inspected objects: (A) Dorsal view (for both underwater and aerial vision) and (B) lateral view (for aerial vision). 1, an above water object: 2, an underwater object. Arrows show directions of light rays from art object to the corresponding high-resolution area of the retina.

The retina of the Amazon river dolphin is a special case. The visual system of this species is adapted to low-transparent turbid water where vision is possible only at short distances. Contrary to all odier investigated cetaceans, the retina of the Amazon river dolphin has only one area of higher ganglion cell density. However. this single area is located not in the center or temporal sector, but in die lower part of the retina, i.e., in die region responsible for the upper part of the visual field (Fig. 7D). In turbid low-transparent water, significant illumination exists only near the water surface, i.e., in the upper part of the visual field of a normally oriented animal. Just this part of the visual field is served by the ventral part of the retina where the Amazon dolphin has higher retinal resolution. The density ol ganglion cells in this region reaches 500 cells/nun2; with the small size of the eyeball, this corresponds to a cell density of about 2 cells/deg\

B. Pinnipeds

Few otariids have been subjects of study of the ganglion cell topography in retinal whole mounts (Mass, 1997). The northern fur seal has a typical area centralis, a well-defined area of high concentration of ganglion cells (Fig. 9A). It is located at a distance of 22-23 nnn (which corresponds to 35-40° of the visual field) from the optic disk; taking into account the position of the eye in orbit, this place may be at the projection of the vertical meridian of the visual field. Thus, the position of this area is similar to that in terrestrial carnivores. Cell density in this area reaches 1000 cells/mm2, which corresponds to more than 160 cells/deg”.

Quite different is the retinal topography in the walrus. The area of increased ganglion cell density is not defined as clearly as in the northern fur seal. It looks like a horizontally extended oval, resembling the visual streak of terrestrial mammals (Fig. 9B). Within this streak, the highest cell density in its temporal part exceeds 1000 cells/mm2; because of the smaller size of the walrus eye, this cell density corresponds to only about 50 cells/deg2. No phocid seals have been studied successfully yet with respect to their retinal topography.

C. Other Marine Mammals

1. Sirenians Ganglion cell distribution in the manatee retina represents an example of low specialization. There is no sharply restricted spot of cell concentration. Ganglion cell distribution is not uniform but varies smoothly across the retina: cell density is higher in a large center part of the retina (except in the nearest vicinity of the optic disk) and diminishes toward the edges (Fig. 9C). The highest cell density is about 250-300 cells/mm2; for a rather small manatee eye, this corresponds to 6-7 cells/deg2.

2. Sea Otters In the sea otter retina ganglion cells topography (Fig. 9D) has a number of features similar to that of terrestrial mammals. The high-density area resembles nasotemporal streak. Within this streak, in its temporal part, there is a narrow and well-defined spot of the highest cell density, which is similar to the area centralis in terrestrial mammals. The highest ganglion cell density in the sea otter exceeds 4000 cells/mm2; in the rather small eye of the sea otter, this corresponds to 50-60 cells/deg2.

D. Estimations of Visual Acuity from Ganglion Cell Density

Visual acuity is determined by two factors: quality of the eye optics and retinal resolution. In normal eyes, these two values are in agreement. Therefore, retinal resolution can be used as a first-order estimate of visual acuity. Retinal resolution depends on the density of ganglion cells (not of other retinal cells, e.g., photoreceptors, as ganglion cells transmit visual information to the brain). Thus, data on ganglion cell topography can be used to estimate the visual acuity of investigated species. When it is possible to compare estimates of visual acuity obtained by behavioral (psychophysical) methods and those based on ganglion cell topography, these estimates are in good agreement.

Retinal resolution (hence, visual acuity) is defined as the mean angular distance between neighboring ganglion cells, i.e., as s = 1/VD, where s is the angular distance between cells and D is the cell density per deg2. The estimation of retinal resolution is different in air and water: if the corneal surface is flat, the retinal image of an object in water is 1.33 times larger than in air (because the ratio of refraction indices of water and air is 1.33). Therefore, retinal resolution in water is 1.33 times better than in air. If the retinal surface is a little convex, this factor is less than 1.33 but still more than 1

Figure 9 Topographic distribution of ganglion cell density in the retina of some pinnipeds, sirenians, and sea otters: (A) the northern fur seal, (B) the walrus, (C) the Caribbean manatee, and (D) the sea otter. Cell density is expressed as number of cells per squared degree of the visual field and is shown by various shadowing, according to the scales. Concentric circles show angular coordinates on a retinal hemisphere centered on the lens. D, V, N, T, dorsal, ventral, nasal, and temporal poles of the retina, respectively. .

Retinal resolution in the areas of the highest concentration of ganglion cells (i.e., visual acuity in the best-vision areas of the visual field) was estimated in a number of marine mammal species (Table I). In many cetaceans (except for river dolphins), it varies from 8 to 12 arc min in water, correspondingly from 11 to 15 arc min in air. For the bottlenose dolphin, the estimation of visual acuity obtained from retinal topography almost coincides with that obtained in behavioral experiments. In general the visual acuity of cetaceans is within a range of visual acuities of many terrestrial mammals, except the foveal vision of primates, where the visual acuity is around 1 arc min. The Amazon river dolphin has much worse visual acuity: 40-50 arc min in water; however. this value is adequate for vision in turbid water where objects are visible at best at a few tens of centimeters.

Among pinnipeds, rather acute vision is characteristic for the northern fur seal: better dian 5 arc min in water and better than 7 arc min in air. This is close to estimates obtained in behavioral experiments in a number of both otariids and phocids: 5-8 arc min (Schusterman, 1972). In the walrus, die visual acuity is worse than in seals: around 8 arc min in water and 10 arc min in air.

In the manatee, underwater visual acuitv is around 20 arc min (it remains unknown whether the manatee has good aerial vision). In the sea otter, the visual acuity is around 7 arc min in water.

VI. Cerebral Visual Centers

In dolphins, the visual system is well represented in the midbrain (the superior colliculus), thalamus (the lateral geniculate body), and in the cerebral cortex. However, the visual centers (both the superior colliculus and the lateral geniculate body) are several times less in volume than corresponding parts of the auditory system (the inferior colliculus and medial geniculate body).

TABLE I

Visual Acuity of Some Aquatic Mammals”

“Visual acuity is presented as the minimal resolvable distance in minutes of arc, rounded to a whole number of minutes. In some cases, a range of variation is indicated (e.g.. 11-12 arc min). Estimates of visual acuity are given for underwater (water) and aerial (air) vision. In the column air. data are not presented when none of the authors attempted to interpret their results in terms of aerial visual acuitv. When several estimates ol visual acuitv in dillerent conditions are available (e.g.. in the nasal and temporal best-vision areas in cetaceans, at various illumination conditions, etc.). the best estimate (i.e.. the minima] resolvable distance) is selected. Mode of measurement: B. behavioral data-. K. data on retinal resolution.

Figure 10 Position of projection sensory areas (visual, auditory, and somatosensory) in the cerebral cortex of cetaceans and pinnipeds: (A) the common bottlenose dolphin and (B) the northern fur seal. Dorsal view of the cerebral cortex. On the right hemisphere, the pattern of cortical sidci and gyri is shown in more detail. On the left hemisphere, only main cortical sulci are shown and the positions of the visual, auditory, and somatosensory areas are indicated. The main sulci (labeled by arrows at their ends): SE, sulcus ectosylvius; SS, s. suprasylvius; SL, s. lateralis; SEL, s. entolateralis; Ssa, s. suprasylvius anterior; Ssp, s. suprasylvius posterior; SPCr, s. postcruciatus. The main gyri (labeled on their surface): GES, gyrus ectosylvius; GSS, g. suprasylvius; GL, g. lateralis; V, visual area (VI, primary projection zone; V2, nonprimary zone); A, auditory area (only a part of this area is visible in B); S, somatosensory area.

In the cerebral cortex of dolphins, visual representation was found by die evoked potential method. This area occupies a part of the cortex named the lateral gyrus (Fig. 10A). The cortical representation of the visual system in dolphins also is not as large as that of the auditory system; nevertheless, it occupies a significant cortical area. There is a differentiation within this area: it contains a zone generating short latency-evoked potentials (i.e., the primary projection zone) and another zone generating evoked potentials of longer latency (a nonprimary zone). The first of them is located in die depth of the entolateral sulcus (a second-order sulcus within the lateral gyrus); the latter occupies the remainder of the lateral gyrus. These two zones differ in cytoarchitectonic features: the primary projection zone contains an incipient layer IV (the layer where visual thalamocortical afferent fibers end), whereas this layer is absent in the nonprimary zone.

In mysticetes, which do not have echolocation, the sizes of visual and auditory structures in the midbrain and thalamus are comparable. Their cortical sensory areas were not investigated.

Among pinnipeds, visual representation in the cerebral cortex was found by the evoked potential method in one otariid species—the northern fur seal (Fig. 10B)—and one phocid species—the Caspian seal, Pusa caspica. The location of this area is very similar to that in carnivores: the projection occupies the caudal part of the lateral gyrus.

VII. Conclusions

In general, the visual system of marine mammals demonstrates a rather high degree of development and performance, in particular, good visual acuity, capabilities to precisely aim visually driven behavior and intermodal transfer, and well-developed visual brain centers. This system also exhibits a number of specific features associated with adaptation to both aquatic and aerial environment, in particular, specific retinal topography (positions of best-vision areas) along with pupil and cornea structure, which provide emmetropia in both air and water.