Adaptive features of aquatic mammals' eye
Abstract
The eye of aquatic mammals demonstrates several adaptations to both underwater and aerial vision. This study offers a review of eye anatomy in four groups of aquatic animals: cetaceans (toothed and baleen whales), pinnipeds (seals, sea lions, and walruses), sirenians (manatees and dugongs), and sea otters. Eye anatomy and optics, retinal laminar morphology, and topography of ganglion cell distribution are discussed with particular reference to aquatic specializations for underwater versus aerial vision. Aquatic mammals display emmetropia (i.e., refraction of light to focus on the retina) while submerged, and most have mechanisms to achieve emmetropia above water to counter the resulting aerial myopia. As underwater vision necessitates adjusting to wide variations in luminosity, iris muscle contractions create species‐specific pupil shapes that regulate the amount of light entering the pupil and, in pinnipeds, work in conjunction with a reflective optic tapetum. The retina of aquatic mammals is similar to that of nocturnal terrestrial mammals in containing mainly rod photoreceptors and a minor number of cones (however, residual color vision may take place). A characteristic feature of the cetacean and pinniped retina is the large size of ganglion cells separated by wide intercellular spaces. Studies of topographic distribution of ganglion cells in the retina of cetaceans revealed two areas of ganglion cell concentration (the best‐vision areas) located in the temporal and nasal quadrants; pinnipeds, sirenians, and sea otters have only one such area. In general, the visual system of marine mammals demonstrates a high degree of development and several specific features associated with adaptation for vision in both the aquatic and aerial environments. Anat Rec, 290:701–715, 2007. © 2007 Wiley‐Liss, Inc.
Comparative studies of the visual system in animals adapted to various living conditions have revealed new specific features of neuronal structures, have aided our understanding of mechanisms of visual perception, and have described the many ways in which sensory systems show adaptations to various environments. In recent years, there has been a great interest in the visual system of aquatic mammals: cetaceans (dolphins, porpoises, and whales), pinnipeds (seals, sea lions, and walruses), sirenians (manatees and dugongs), and sea otters. These species demonstrate various extents of adaptation to the aquatic environment. Many aquatic mammals (cetaceans, sirenians) spend their entire life in the water; however, air‐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 visual systems of these groups feature remarkable morphological and functional specializations for both underwater and aerial vision that are apparent in the optics, retina, and other eye structures.
EYE ANATOMY AND OPTICS
Cetaceans
The structure of the eyecup and the refractive structures of the eye in cetaceans are determined primarily by the optical properties of the aquatic medium and by several other factors: low temperature and low luminosity at depth, strong light scatter by particles (plankton and others) suspended in water, and so on. Therefore, ocular anatomy and optics in cetaceans are significantly different from those in terrestrial mammals.
Characteristic examples of eye structure in cetaceans are presented in Figure 1A–D. Prominent features typical for all cetaceans are a thick sclera (particularly so in baleen whales, or mysticetes, Fig. 1C), a significantly thickened cornea, a highly developed choroid, a highly developed vascular network forming a typical rete mirabilia that fills a significant part of the orbit behind the eyeball, and massive ocular muscles. All these structures take part in protecting the eye from underwater cooling and mechanical damage.

A–D: Schematic presentation of eye anatomy and optics in some cetaceans: the bottlenose dolphin (A), beluga (B), grey whale (C), and Amazon river dolphin (D). Co, cornea; L, lens; Ir, iris; O, operculum; S, sclera; Ch, choroids; R, retina; ON, optic nerve; OD, optic disc. Black arrows delimit a part of the eyecup that can be approximated by a spherical segment of approximately 150 degrees.
The shape of the eyeball is markedly altered as compared with terrestrial mammals. While the eyecup in terrestrial mammals is typically almost spherical, there is substantial flattening of the anterior segment in cetaceans. As a result, the axial length of the eyecup is much smaller than its diameter. As a first approximation, the eyecup shape is close to a hemisphere. More precisely speaking, the shape approximates not a complete hemisphere, but a segment of a sphere of a large arc of approximately 150 degrees, as delimited by arrows in Figure 1A–C.
The cornea in cetaceans is much thicker than in humans and most terrestrial mammals, and its thickness is not uniform. The cornea is thinner in the center and thicker at the periphery. This finding is characteristic of both odontocetes (toothed whales) and mysticetes (baleen whales) (Pütter, 1903; Rochon‐Duvigneaud, 1940; Mann, 1946; Dawson, 1980; Pardue et al., 1993; van der Pol et al., 1995; Mass and Supin, 2002). In the beluga (Delphinapterus leucas), this peripheral thickening forms a characteristic limb at its edges attached to the sclera (Fig. 1B). Although the role of the cornea in light refraction in the cetacean eye is not as crucial as in terrestrial mammals, it does contribute to refraction. The outer corneal surface has lower curvature than the inner surface (Kröger and Kirschfeld, 1992, 1993, 1994; van der Pol et al., 1995). Thus, under water, the cornea acts as a weak divergent lens. The total refraction of the cornea and lens makes the cetacean eye well emmetropic (i.e., light is refracted so that it is focused on the retina) within a range of ±1 diopters under water (Kröger and Kirschfeld, 1994).
In terrestrial mammals, the convex outer surface of the cornea is the major refractive unit of the eye because it separates media with different refractive indices: air with a refractive index of approximately 1, and the corneal and underlying tissues with refractive indices of 1.33–1.35. In cetaceans, the refractive index of the cornea is approximately 1.37 (Dawson et al., 1972; Kröger and Kirschfeld, 1994). Nevertheless, this refractive index is little different from that of water (1.33–1.34). As a result, the corneal surface takes a 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 (Sivak, 1980). This is why the lens is almost spherical in most cetaceans or, as in a few mysticetes and the beluga whale, of a slightly elliptical shape (see Fig. 1). The curvature of the lens surface provides sufficient refractive power to focus images on the retina, despite the very weak refractive power of the cornea in water. It is not surprising that cetacean optics are similar to those of fish, thus reflecting the common environmental constraints of the optical properties of water.
A strongly convex (spherical) lens consisting of homogeneous material should have a 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 (Rivamonte, 1976; Kröger and Kirschfeld, 1993).
In the cetacean eye, the spherical lens is positioned so 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. These optics are significantly different from that in terrestrial mammals, in which the best focusing occurs on the eye axis.
The spherical shape of the lens in cetaceans led to loss of the accommodation mechanism typical of terrestrial mammals—that is, change of the lens shape by the ciliary muscle. The ciliary muscle is poorly developed in all dolphins and is absent from most whales (Waller, 1984; West et al., 1991; Bjerager et al., 2003), suggesting that accommodation cannot be achieved by a change of the lens shape (Dral, 1972). This suggestion is supported by ophthalmoscopic observations (Dawson et al., 1987b), which revealed no significant accommodative changes. It has, however, been suggested that accommodation in cetaceans does occur 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 massive musculus retractor bulbi, which produces axial displacements of the globe of the eye within 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 thus shifting the lens backward (Kröger and Kirschfeld, 1989).
Adaptation of the cetacean eye to underwater vision is also evident in the structure of the iris and pupil. Cetacean vision is affected by wide and rapid changes in brightness when the animal dives from the well lit water surface into depths where the light level is very low. This change requires the pupil to react to a wide range of illuminations and, therefore, to express a wide range of sizes. The cetacean pupil has an unusual shape. The upper part of the iris has a characteristic protuberance called the operculum. At low illumination, the operculum is contracted (raised), so the pupil, similarly to other mammals, is round or slightly oval (Fig. 2A). With increasing light exposure, the operculum advances downward, turning the pupil into a U‐shaped slit (Fig. 2B). At high illumination, the slit becomes closed, leaving only two narrow holes in the temporal and nasal parts of the iris (Fig. 2C) (Dawson et al., 1979; Herman et al., 1975). This pupil shape is characteristic of many odontocetes, including the bottlenose dolphin (Tursiops truncatus), harbor porpoise (Phocoena phocoena), common dolphin (Delphinus delphis), tucuxi (Sotalia fluviatilis), beluga (Delphinapterus leucas) (see review in Supin et al., 2001), and sperm whales (Physeter macrocephalus) (Rochon‐Duvigneaud, 1940; Bjerager et al., 2003). This pupil shape is also characteristic of the gray whale (Eschrichtius robustus) (Mass and Supin, 1997) and some other mysticetes (Zhu et al., 2000). The only exception was the Amazon river dolphin (Inia geoffrensis), which has a round pupil like most terrestrial mammals.

A–C: Shape of the pupil in the bottlenose dolphin at various levels of illumination: low illumination, nonconstricted oval pupil (A); moderate illumination, partially constricted U‐shaped pupil (B); high illumination, strongly constricted pupil reduced to two pinholes (C).
The cetacean eye is emmetropic in water, however, in air, the refraction on the outer convex corneal surface adds to the lens refraction. The difference in refractive indices between air and the cornea increases the refractive power of the most convex central part of the corneal surface by approximately 20 diopters (Dral, 1972; Dawson et al., 1987b). The addition of this refraction to the emmetropic lens refraction should make the cetacean eye catastrophically myopic (near‐sighted) in air. However, this myopia is countered by the presence of flattened (low‐curvature) regions of the cornea. Keratoscopic studies in bottlenose dolphins showed a “spoon” shape of the cornea with lower curvature in its nasal and temporal regions (Dawson et al., 1987b). Their refractive power is low enough and may be compensated by accommodation. Another model, however, suggests that myopia in air does not arise because vision in water and in air uses different parts of the lens with different refraction indices (Rivamonte, 1976). An additional correction for aerial myopia can be provided by constriction of the pupil. Above water, diurnal luminosity is high and evokes strong constriction of the pupil, which to a large extent corrects errors of refraction, including aerial myopia, astigmatism, and spherical aberrations in the lens.
Another adaptation of the cetacean eye to conditions of low luminosity is a highly developed reflective layer, the tapetum lucidum. The tapetum is present in all cetaceans, and it is especially well developed in mysticetes. It lies behind the retinal pigment epithelium within the choroid. The structure of the tapetum and its properties has been described in several cetaceans (Dawson, 1980; Young et al., 1988). In cetaceans, the tapetum is formed with extracellular collagen fibrils (tapetum fibrosum). Multiple reflection of light from 50–70 layers of fibrils results in significant light reflection back to the retina. In all cetaceans, the tapetum covers at least the upper two thirds of the fundus (Dawson, 1980), and in some whales, it covers the entire fundus (Waller, 1984). Such complete coverage of the fundus by the tapetum in cetaceans is unique among mammals; in terrestrial mammals, the tapetum does not usually extend below the horizontal equator of the eye (Prince, 1956).
Pinnipeds
The visual system of pinnipeds features adaptation to both aquatic and terrestrial habitats (Jamieson and Fisher, 1972; Supin et al., 2001; Griebel and Peichl, 2003). Eye anatomy in pinnipeds, despite notable difference from cetaceans, has some common features reflecting adaptation to underwater vision (Fig. 3A,B) (Jamieson and Fisher, 1972; Mass, 1992; Mass and Supin, 1992, 2003, 2005). 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. This allows much of the retina to be equidistant from the lens center. Thus, the eye optics, as in cetaceans, is almost centrally symmetrical.

A–D: Schematic presentation of eye anatomy and optics in some pinniped, the manatee and sea otter: the northern fur seal (A), the harp seal (B), the manatee (C), and the sea otter (D). Co, cornea; FC, flattened region of the cornea; L, lens; Ir, iris; PL, pectinate ligament; CB, ciliary body; S, sclera; Ch, choroids; R, retina; ON, optic nerve; OD, optic disc; P, protuberance of the lens.
The iris in pinnipeds is very muscular and heavily vascularized. The dilatator muscle is well developed. Most pinnipeds have a pupil that becomes pear‐shaped when constricted. An exception is the diagonal pupil in Erignathus barbatus. Pupil size can change over a very wide range and, at bright illumination, it constricts to a very small hole. In shallow‐diving species, the range of pupillary area variation is rather small: 70.5 times in the harbor seal (Phoca vitulina), and 26 times in the California sea lion (Zalophus californianus). In a deep diver, the northern elephant seal (Mirounga angustirostris), the pupil area varied within an extremely wide range, from a giant area of 422 mm2 in dark‐adapted conditions (approximately 23 mm in diameter) to a pinhole opening of 0.9 mm2 in light‐adapted conditions, that is, the range of variation is almost 470 times (Levenson and Schusterman, 1997).
The ciliary muscle in pinnipeds is much better developed than in cetaceans (Jamieson and Fisher, 1972; Sivak et al., 1989; West et al., 1991), although accommodation is weak or absent (Sivak et al., 1989).
Unlike cetaceans, the central part of the cornea in pinnipeds, both otariids and phocids, has a clearly delimited region (6–10 mm in diameter) of almost flat surface. It is located near the center of the cornea (FC region in Fig. 3A). The flat region of the cornea serves as an emmetropic “window” in which refraction remains almost equal both in water and air. The presence of this flat region was demonstrated by precise measurements in the Californian sea lion (Dawson et al., 1987b). In another pinniped, the hooded seal (Cystophora cristata), the flattened part of the cornea does not look like a delimited region, but rather arises because of low curvature of the cornea of their extremely large eyeball (Sivak et al., 1989).
From the point of view of eye construction, the presence of a flattened region of the cornea in pinnipeds is a very intriguing feature. 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 the flat cornea suggests that this pressure is very low, perhaps approximately zero. Anatomical observations on the northern fur seal showed that its vitreous body is a rigid rather than a gelatinous consistency, thus indicating a major role in maintenance of eyeball shape and dimensions (authors' observation).
One more adaptation of the pinniped eye to underwater vision in conditions of low luminosity is a highly developed reflective layer, the tapetum. The pinniped tapetum is one of the best developed among both terrestrial and aquatic mammals (Walls, 1942). Contrary to cetaceans, the tapetum in pinnipeds is formed with intracellular reflective rodlets (tapetum cellulosum) (Braekevelt, 1986). It consists of 20 to 34 layers, and covers a large proportion of the fundus (Nagy and Ronald, 1970, 1975; Jamieson and Fisher, 1971).
Sirenians
Sirenians (the order Sirenia) are a group of completely aquatic mammals adapted to an herbivorous lifestyle. Among only a few species of this order (the West Indian manatee, Trichechus manatus; the Amazonian manatee, T. inunguis; the West African manatee, T. senegalensis; and the dugong, Dugong dugong), only two former species were studied to some extent in respect of their vision. The eye anatomy was described in the Amazonian manatee (Trichechus inunguis) by Piggins at al. (1983), and in the Florida manatee (Trichechus manatus latirostris, a subspecies of the West Indian manatee) by Mass et al. (1997). In both T. manatus and T. inunguis, the eye is rather small (13–19 mm diameter) and is set deeply within the ocular fascia. In general, the eye morphology resembles that of terrestrial mammals more than cetaceans (Fig. 3C). 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. The lens is of lenticular shape, but the small lens size allows a curvature that is strong enough for underwater refraction without the contribution of corneal refraction. Contrary to the majority of mammal species featuring avascular corneas, blood vessels have been found throughout the cornea of the manatee (Harper et al., 2005). However, the size, density and location of the vessels are too small to affect markedly the manatee's vision. The sclera is thin. Thus, despite a completely aquatic mode of life, the eye anatomy of the manatee retains several conservative features. Underwater, the eye is almost emmetropic or slightly hyperopic, but in air the eye is strongly myopic. It remains unknown whether the manatee has some mechanisms to compensate for aerial myopia; thus, its capability for aerial vision remains unknown.
Sea Otters
The sea otter (Enhydra lutris), a member of the Mustelidae family, represents an example of transition of terrestrial carnivores to an aquatic life style. Inhabiting the coastal zone and searching for prey under water, sea otters need to have good vision both in air and water. The ocular anatomy of the sea otter is shown in Figure 3D (Murphy et al., 1990; Mass and Supin, 2000). To a large extent, the eyeball is similar to those of terrestrial mammals: it is almost spherical, axial length is only a little shorter than the diameter. Contrary to spherical lenses of cetaceans and pinnipeds, the sea otter's lens 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 enables emmetropia both in air and water (Murphy et al., 1990).
RETINAL LAMINAR MORPHOLOGY
Cetaceans
The laminar structure of the retina was investigated in a variety of cetacean species, including bottlenose dolphin (Tursiops truncatus) (Perez et al., 1972; Dawson and Perez, 1973; Dral, 1975a, b, 1977; Dawson, 1980; Dawson et al., 1982), common dolphin (Delphinus delphis) (Dral, 1983), Dall's porpoise (Phocenoides dalli) (Murayama et al., 1992a, 1995), beluga (Delphinapterus leucas) (Pütter, 1903; Pilleri, 1964), pilot whale (Globicephala melaena) (Peichl et al., 2001), fin whale (Balaenoptera physalus) (Pilleri and Wandeler, 1964), and minke whale (B. acutorostrata) (Murayama et al., 1992a, b). The laminar structure of the retina in all cetaceans is qualitatively similar to that in terrestrial mammals (Fig. 4A,B). It consists of the receptor layer, outer nuclear layer, outer plexiform layer, inner nuclear layer, inner plexiform layer, ganglion cell layer, and, finally, the optic‐fiber layer. Even in a cetacean species with strongly reduced visual system, the Ganges river dolphin (Platanista gangetica), which has almost no lens and no oculomotor muscles, the laminar structure of the retina shows no radical changes and contains all the layers (Dral and Beumer, 1974; Purves and Pilleri, 1974).

A,B: Microphotographs of transverse sections of the retina of a bottlenose dolphin (A) and a grey whale (B). RL, receptor layer; ONL, outer nuclear layer; OPL, outer plexiform layer; INL, inner nuclear layer; IPL, inner plexiform layer; GL, ganglion cell layer. Giant ganglion cells are visible in the ganglion layer.
Although qualitatively similar to other mammals, the laminar structure of the retina in cetaceans markedly differs quantitatively. The cetacean retina is much thicker than that of terrestrial mammals, reaching up to 425 μm (Dral, 1977; Dawson et al., 1982; Murayama et al., 1995). For comparison, the thickness of the retina in diurnal terrestrial mammals is 110–220 μm (Prince et al., 1960).
The receptor layer of the retina in all cetaceans thus far studied consists predominantly of rods. The question of existence of cones remained debatable for some time. The first study of the laminar structure of the retina in the bottlenose dolphin (Tursiops truncatus) using Golgi preparations (Perez et al., 1972) as well as subsequent publications (Dawson and Perez, 1973; Dral and Beumer, 1974) reported different receptor profiles in the receptor layer and different sizes of photoreceptor endings in the outer plexiform layer, which are indicative of different receptor types. Later, a small number of large conelike units embedded among numerous small round units were described (Dawson, 1980). Similar data were obtained by light microscopy in the Dall's porpoise (Phocoenoides dalli) (Murayama et al., 1995) and pilot whale (Globicephala melaena) (Peichl et al., 2001). Two types of receptors were also seen by electron microscopy in the retina of the Amazon river dolphin (Inia geoffrensis) (Waller, 1982). Recent studies of visual pigments have shown that long‐wave sensitive L‐cone opsin does exist in receptors of the retina in the bottlenose dolphin (Tursiops truncatus) (Fasick et al., 1998; Fasick and Robinson, 1998, 2000). It is assumed now that the cetacean retina does contain cone receptors, however, rods dominate; cone proportion is in the range of 1% (Peichl et al., 2001). The cone density observed in marine mammals (3,000–7,000/mm2 up to 10,000/mm2 in the harbor porpoise, Phocoena phocoena) is close to that of nocturnal terrestrial mammals (2,200–7,000/mm2, Peichl et al., 2001).
Contrary to the majority of terrestrial mammals, which have two types of cones with different pigments providing color vision (short‐wave sensitive S‐opsin and middle‐to‐long‐wave sensitive L‐opsin), only L‐opsin containing cones were found in the cetacean retina (Peichl et al., 2001). Immunocytochemical studies using antibodies against the S‐opsin have reported a complete absence of the S‐opsin in 10 species of odontocetes while confirming the presence of L‐cones in all these species (Peichl and Berhmann, 1999; Peichl et al., 2001). These data suggest that cetaceans are L‐cone monochromats and, hence, should lack the dichromatic color vision typical of most terrestrial mammals. However, some data indicate that the rod pigment may contribute to the spectral sensitivity function (Fasick et al., 1998), so residual colour vision in cetaceans could be achieved in mesopic conditions by exploiting the signal differences between the L‐cones and rods (Griebl and Peichl, 2003).
A detailed description of the structure of the outer nuclear layer, the outer plexiform layer, the inner nuclear layer, and the inner plexiform layer, based on Golgi preparations of the bottlenose dolphin (Tursiops truncatus) retina, was reported by Perez et al. (1972), and a similar description was reported for other cetacean species by Dawson (1980). According to these descriptions, amacrine, bipolar, and horizontal cells are generally similar to those in terrestrial mammals. The inner plexiform and ganglion cell layers of the retina demonstrate the most prominent difference between terrestrial mammals and cetaceans. Particularly, the ganglion cell layer in cetaceans differs from that of terrestrial mammals.
Ganglion cells have been described in most detail using Golgi preparations in the common dolphin (Delphinus delphis) and bottlenose dolphin (Tursiops truncatus) (Shibkova, 1969; Perez et al., 1972; Dawson et al., 1982). The ganglion layer of cetaceans consists of a single row of large neurons. The only exception is the sperm whale (Physeter macrocephalus): its giant ganglion cells form multiple layers (Bjerager et al., 2003). Apart from large cell sizes, a characteristic feature of the ganglion layer in cetaceans is low cell density. The large neurons are separated by wide intercellular spaces. This cell pattern was described in Nissl‐stained retinal transverse sections from the beluga whale (Delphinapterus leucas) (Pütter, 1903; Pilleri, 1964), fin whale (Balaenoptera physalus) (Pilleri and Wandeler, 1964), and Dall's porpoise (Phocoenoides dalli) (Murayama et al., 1995) as well as in retinal whole‐mounts from the same species (Dral, 1977, 1983; Mass and Supin, 1986, 1995; Murayama et al., 1995), the gray whale (Eschrichtius robustus) (Mass and Supin, 1997), minke whale (Balaenoptera acutorostrata) (Murayama et al., 1992a), and beluga (Delphinapterus leucas) (Mass and Supin, 2002).
Both Golgi preparations and Nissl‐stained whole‐mounts revealed large neuron bodies with a clear membrane, a large amount of cytoplasm, a clearly visible nucleus of up to 15 μm in diameter, and light nucleolus of 4 to 5 μm in diameter. Cell bodies contained easily visible, intensely stained Nissl granules. All large neurons (particularly giant neurons of the whale retina) showed several axon/dendrite bases.
A remarkable feature of the cetacean retina is the presence of extremely large, giant ganglion cells. Most ganglion cells in the cetacean retina are of rather large size, but giant cells reach 50–80 μm and more. These large neurons have been described in many studies of several dolphin species: in the bottlenose dolphin (Tursiops truncatus) (Perez et al., 1972; Dawson et al., 1982; Mass and Supin, 1995), common dolphin (Delphinus delphis) (Dral, 1983), harbor porpoise (Phocoena phocoena) (Mass and Supin, 1986), Dall's porpoise (Phocoenoides dalli) (Murayama et al., 1995), Chinese river dolphin or baiji (Lipotes vexillifer), and finless porpoise (Neophocaena phocaenoides) (Gao and Zhou, 1987), and in a few mysticete species (Pilleri and Wandeler, 1964; Murayama et al., 1992a, b; Mass and Supin, 1997).
It should be noted that the term giant as applied to terrestrial mammals suggests a ganglion cell size between 15–35 μm, including parts of dendrites (Fukuda and Stone, 1974; Hebel and Hollander, 1979; Hughes, 1981). In cetaceans, however, the size of just the ganglion cell body alone can exceed 75 μm.
In some cetacean species, ganglion cells do not reach such large sizes. In the Amazon river dolphin (Inia geoffrensis), the largest ganglion cells do not exceed 40–42 μm (Waller, 1982; Mass and Supin, 1989); in the retina of the Ganges river dolphin (Platanista gangetica), ganglion cells larger than 20 μm were not found (Dral and Beumer, 1974). However, even these cells are markedly larger than ganglion cells in many terrestrial mammals.
Quantitative characterization of ganglion cell body sizes was provided in studies of the cell‐size distributions in various parts of the retina. Figure 5 presents frequency vs. size histograms for ganglion cells in retinae of bottlenosed dolphin (Tursiops truncatus) (Fig. 5A,B), gray whale (Eschrichtius robustus) (Fig. 5C,D), and tucuxi dolphin (Sotalia fluviatilis) (Fig. 5E,F) (Mass and Supin, 1995, 1997, 1999) in parts of the retina with high and low concentration of ganglion cells. The histograms show that the most probable cell size is 20 to 35 μm, although cells as large as 50–60 μm are also present, and there are no cells smaller than 8–12 μm. Large cells, over 35 μm, are present mainly in low‐density areas; in high‐density zones these cells are rare. The large size of ganglion cells, mainly 20 to 30 μm or more, is also characteristic of retinas of other cetacean species: the harbor porpoise (Phocoena phocoena) (Mass and Supin, 1986), Amazon river dolphin (Inia geoffrensis) (Mass and Supin, 1989), minke whale (Balaenoptera acutorostrata) (Murayama et al., 1992a, b), and Dall's porpoise (Phocoenoides dalli) (Murayama et al., 1995).

A–D: Histograms showing size distributions of ganglion cells in the retina of cetaceans: the bottlenose dolphin, areas of high and low ganglion cells density, respectively (A,B); the same for the grey whale (C,D); the same for the riverine tucuxi (E,F).
The size histograms of cetacean's ganglion cells are monomodal; however, the “tail” represents cells larger than 40–45 μm. This tail contains a small part of the total cell population. For example, in the bottlenose dolphin (Tursiops truncatus), cells larger than 40 μm constitute approximately 4% of the total cell number in the high‐density areas and up to 16% in the low‐density areas (Fig. 5A,B; Mass and Supin, 1995); in the beluga (Delphinapterus leucas) (Mass and Supin, 2002) and grey whale (Eschrichtius robustus) (Mass and Supin, 1997), the tail of distributions is negligible (Fig. 5C,D). In the tucuxi dolphin (Sotalia fluviatilis), the largest cells (36–59 μm) are more numerous: up to 13% and 25% in the high‐ and low‐density areas, respectively, and the cell‐size distribution is polymodal (Fig. 5E,F) indicating at least three groups of ganglion cells with sizes 8 to 20 (small), 21 to 35 (large), and 36 to 59 μm (giant) cells (Mass and Supin, 1999). In the Chinese river dolphin or baiji (Lipotes vexillifer), the ganglion cell sizes were reported as distributed in a bimodal manner with peaks at 13 and 40 μm (Gao and Zhou, 1987).
To date, there is no commonly adopted explanation of why giant ganglion cells are characteristic of the cetacean retina. It is possible that giant ganglion cells, with their thick axons that conduct nerve spikes at high velocity, facilitate fast signal transmission through long nerve pathways in a large body. However, large terrestrial mammals (for example, cattle or elephants) have retinal ganglion cells of no more than 25–30 μm (Hebel and Hollander, 1979; Stone and Halasz, 1989).
Pinnipeds
Laminar organization of the retina in pinnipeds (Fig. 6A,B) generally corresponds to that of terrestrial mammals (Landau and Dawson, 1970; Nagy and Ronald, 1970, 1975; Jamieson and Fisher, 1971; Welsch et al., 2001; Mass and Supin, 2005). However, there are several features unique to aquatic mammals.

A,B: Microphotographs of transverse sections of the retina of a Steller sea lion (A) and a Baikal seal (B). Designations as in Figure 4. A giant ganglion cell in the ganglion layer and large horizontal cells in the inner nuclear layer are visible in (A).
As in terrestrial carnivores with nocturnal vision, the receptor layer of the retina in all pinnipeds thus far studied consists predominantly of rods, with their slender, nearly cylindrical, long outer segments densely packed. The outer limiting membrane is clearly discernible between the photoreceptor and outer nuclear layers. The outer nuclear layer is composed of receptor pericarya arranged in a multilevel manner. This layer is the thickest of all the layers, being more than 20 pericarya deep.
The question of existence of cones has been a matter of discussion for a long time. In early studies of the pinniped retina, cones were not found (Landau and Dawson, 1970; Nagy and Ronald, 1970). Later investigations using light and electron microscopy demonstrated the presence of two types of photoreceptors, presumably rods and cones, in the harbor seal (Phoca vitulina) (Jamieson and Fisher, 1971) and harp seal (Pagophilus groenlandicus) (Nagy and Ronald, 1975). Recently, immunochemical studies in five species of seals and sea lions demonstrated that their retinae contained sparse populations of cones, comprising approximately 1% of the photoreceptors (Peichl et al., 2001). The cone density varies among species within a range of 3,000 to 7,000/mm2 up to 10,000/mm2 in the ringed seal (Pusa hispida) (Peichl et al., 2001), which is close to nocturnal terrestrial mammals. However, these studies revealed only one opsin type in the cone receptors, the middle‐to‐long‐wave sensitive L‐opsin (Peichl and Moutairou, 1998) and did not reveal the short‐wave sensitive S‐opsin. This feature is common in cetaceans (despite the very different phylogenies of cetaceans and pinnipeds), and distinguishes pinnipeds from the majority of terrestrial mammals that have at least two spectrally sensitive cone types (middle‐ and short‐wave sensitive) or three cone types in primates (Jacobs, 1993).
The inner nuclear layer in pinnipeds is thin and rather chaotically organized. There are giant horizontal cells within the layer. The bipolar and amacrine cells are diffusely distributed. Only slight ordering can be seen near the outer and inner plexiform layers. This finding contrasts with terrestrial mammals, in which this layer is strictly ordered. All reports noticed very large horizontal cells within the inner nuclear layer in the harp seal (Pagophilus groenlandicus) (Nagy and Ronald, 1970), harbor seal (Phoca vitulina) (Jamieson and Fisher, 1971), and Steller sea lion (Eumetopias jubatus) (Mass and Supin, 2005). Giant processes of these cells spread to a large distance. These giant horizontal cells are distributed irregularly in the close vicinity of bipolar as well as amacrine cells. Bipolar cells typically are of a round shape with oval nuclei and diffuse chromatin filaments. Amacrine cells are large and irregular in shape; they are located close to the inner plexiform layer.
The ganglion layer consists of a single row of rather large ganglion cells separated by wide intercellular spaces. A majority of ganglion cells are as large as 12–35 μm with a separate group of giant cells larger than 35–40 μm (Fig. 7A–D). In the northern fur seal (Callorhinus ursinus), ganglion cells are mostly of 14 to 28 μm with the largest cells up to 50 μm (Mass and Supin, 1992); in the Steller sea lion (Eumetopias jubatus), the majority of cells are 10 to 25 μm with some cells are as large as 37 μm (Mass and Supin, 2005); in the harp seal (Pagophilus groenlandicus), typical cells are 20 to 30 μm with some cells were as large as 60 μm (Nagy and Ronald, 1970; Mass and Supin, 2003). Giant ganglion cells were noticed also in the retina of the harbor seal (Phoca vitulina) (Jamieson and Fisher, 1971). The percentage of giant cells (8–10% in the northern fur seal, 5–6% in the harp seal, 8% in the Steller sea lion) is close to corresponding proportions of α‐cells described in other mammals: from 1 to 10% (Peichl, 1991). The similarity of giant cells in pinnipeds to ganglion α‐cells described in retinas of terrestrial mammals seems obvious. Such cell body sizes are not typical of terrestrial carnivores, which have very few ganglion cells larger than 25–30 μm (Fukuda and Stone, 1974; Hughes, 1981; Wong and Hughes, 1987).

A–D: Histograms showing size distributions of ganglion cells in the retina of pinnipeds and the sea otter: the northern fur seal, areas of high and low ganglion cells density, respectively (A,B); the same for the harp seal (C,D); the same for the sea otter (E,F).
Sirenians
Data on retinal organization of sirenians are rare. The first description of the manatee's retina was published by Pütter (1903). Rochon‐Duvigneaud (1943) and Walls (1942) described the retina of the manatee and dugong as pure rod. Later, Piggins et al. (1983) also pointed out that the manatee's retina has a structure typical of nocturnal animals and that cones are rare or absent. Ganglion cells were noticed to be few in number, although their number was not estimated quantitatively. A detailed description of the retina of Trichechus manatus was made by Cohen et al. (1982), who established that the laminar structure of the retina is fully developed. Using light and electron microscopy, they have found both rodlike and conelike photoreceptors. Moreover, two cone subclasses were found, which indicated a possibility of color vision.
Sea Otters
Retinal organization in the sea otter (Enhydra lutris) exhibits more properties in common with terrestrial than with aquatic mammals. It seems to represent an early stage of adaptation of the mammalian visual system to an aquatic mode of life, although the eye is capable of functioning well in both air and water.
Contrary to aquatic and similarly to terrestrial mammals, majority of ganglion cells in the sea otter's retina are rather small, of 8 to 18 μm, mostly 11–15 μm in the retinal area of high ganglion cell density, up to 28 μm in the peripheral area of low cell density (Fig. 7E,F); only 6% of cells are larger than 30 μm (Mass and Supin, 2000). Mean cell size in the high‐density streak in the sea otter's retina (11–15 μm) is also close to that of terrestrial mammals. In the retinal periphery, cell size distribution reveals three distinctive size groups: 8–18, 17–28, and 29–47 μm (Fig. 7F), whereas the temporal high‐density area contains only small cells (Fig. 7E). Proportion and distribution of these three groups in the sea otter is close to those of α‐, β‐, and γ‐cells in the cat (Hughes, 1981; Stone, 1983; Peichl, 1991) and the ferret (FitzGibbon et al., 1996).
TOPOGRAPHY OF GANGLION CELL DISTRIBUTION
Cetaceans
Ganglion cells are distributed nonuniformly in the mammal retina; the concentration of ganglion cells (number of cells per area unit) in some retinal areas is low, whereas in other areas it is much higher. Regions of high ganglion cell concentration are of special interest because they provide the most detailed analysis of visual images.
Characteristics of retinal topography in a variety of mammals are presented in reviews by Stone (1983) and Hughes (1977). In terrestrial mammals, there are two main types of organization of a region with high cell density. Mammals with frontal vision have a fovea, or area centralis, located in the center of the visual field. This retinal area is largely avascularized 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 called the visual streak. Some marsupials have both a separate visual streak and an area centralis.
For a long time, the existence of regions of ganglion cell concentration in the cetacean retina was questioned. This doubt was because the cetacean retina does not have an avascular or low vascularized area, which indicates the presence of the fovea or area centralis in terrestrial mammals and humans. Therefore, visual examination of the fundus did not reveal anything that could be interpreted as a fovea‐like region (Dawson et al., 1987a).
Detailed data on the retinal topography in dolphins were obtained when retinal whole‐mounts (flat mounts) became used for investigation of distribution of ganglion cells. Several cetacean species were investigated using the retinal whole‐mount method, mostly marine odontocetes: the common dolphin (Delphinus delphis) (Dral, 1983), bottlenose dolphin (Tursiops truncatus) (Dral, 1975a, 1977; Mass and Supin, 1995), harbor porpoise (Phocoena phocoena) (Mass and Supin, 1986), Dall's porpoise (Phocoenoides dalli) (Murayama et al., 1995), tucuxi dolphin (Sotalia fluviatilis) (Mass and Supin, 1999), pacific white‐sided dolphin (Lagenorhynchus obliquidens) (Murayama and Somiya, 1998), and beluga whale (Delphinapterus leucas) (Murayama and Somiya, 1998; Mass and Supin, 2002). These studies revealed the presence of distinctive areas of ganglion cell concentration in the cetacean retinas; in these areas, the ganglion cell density much exceeded that of other retinal regions (Fig. 8A,B).

A,B: Microphotographs of the ganglion layer in a retinal whole‐mount of a bottlenose dolphin: an area of high cell density (A) and an area of low cell density (B).
The most characteristic feature of all these dolphin species was that, unlike all the studied terrestrial mammals, marine dolphins have not just one area of high ganglion cell density, but rather two such areas (Fig. 9A–C). The high‐density areas are located at the horizontal diameter of the retina, one in its nasal sector and the other in the temporal sector. In the bottlenose dolphin (Tursiops truncatus), both these areas are located at a distance of 15–16 mm from the optic disk, which corresponds to 50–55 degrees of the visual field. Ganglion cell density is almost equal in each of these areas. It reaches 700–800 cells/mm2 (Fig. 9A), 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.

A–D: Topographic distribution of ganglion cell density in the retina of some cetaceans: the bottlenose dolphin (A), the riverine tucuxi (B), the grey whale (C), and the Amazon river dolphin (D). Cell density is expressed as number of cells per mm2 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.
In other dolphin and porpoise species, the retinal topography is generally similar to that described above for Tursiops in having two areas of high ganglion cell density. In some cetacean species, however, the cell density in the temporal area (i.e., the region serving the frontal visual field) is higher than in the nasal region. Species with this morphology include: the harbor porpoise (Phocoena phocoena) (Mass and Supin, 1986), Dall's porpoise (Phocoenoides dalli) (Murayama et al., 1992a, 1995), beluga whale (Delphinapterus leucas) (Mass and Supin, 2002), and false killer whale (Pseudorca crassidens) (Murayama and Somiya, 1998). Although similar qualitatively, ganglion cell density varies quantitatively between species. For example, in the riverine tucuxi (Sotalia fluviatilis), the ganglion cell density does not exceed 200 cells/mm2 (Fig. 9B); in the small tucuxi eyeball, this value corresponds to a rather low density per squared degree, not more than 5–6 cells/deg2 (Mass and Supin, 1999).
Retinal topography of ganglion cells was also studied in two mysticete species: the gray whale (Eschrichtius gibbosus) (Mass and Supin, 1997) and minke whale (Balaenoptera acutorostrata) (Murayama et al., 1992a, b). These mysticetes also have ganglion cell distributions with two areas of high cell density, in the nasal and temporal sectors. Note that ganglion cell density in the grey whale (up to 200 cells/mm2, Fig. 9C) is almost the same as in the riverine tucuxi; but in the large eyeball it corresponds to a density up to 30 cells/deg2. Again, the cell density in the temporal area is a little higher than in the nasal area. Thus, the pattern of ganglion cell distribution with two high‐density areas can be considered as a common feature of many cetaceans, both odontocetes and mysticetes.
The Amazon river dolphin (Inia geoffrensis) presents a specific case of topographical organization of the retina. The Amazon river dolphin has only one area of increased ganglion cell density (Fig. 9D). However, contrary to terrestrial mammals, this area is located not in the central part of the retina, but in the ventral part—that is, in the region responsible for the upper portion of the visual field (Mass and Supin, 1989). The density of ganglion cells in the high‐density area of the Amazon river dolphin reaches 400–500 cells/mm2; with the small size of the eyeball, this value corresponds to a density of less than 3 cells/deg2 when projected onto the visual field.
A question arises whether the difference between marine cetaceans (marine dolphins and whales) and the Amazon river dolphin in their retinal topography is associated with their different systematic position (the Amazon river dolphin belongs to the Iniidae family) or with their visual ecology (the Amazon river dolphin inhabits river water, which is much less transparent than sea water). A comparison with the riverine tucuxi (Sotalia fluviatilis) (Mass and Supin, 1999), finless porpoise (Neophocoena phocoenoides) and the baiji (Lipotes vexillifer) (Gao and Zhou, 1987), which also inhabit turbid river waters, shows that just the systematic position of the Amazon river dolphin determines the specific organization of its ganglion layer.
Because the presence of two high cell‐density areas in the retina widely occurs among cetaceans, a question arises as to the functional significance of this mode of retinal organization. The presence of the two areas of high ganglion cell density (i.e., of high retinal resolution) may be associated with the cetacean's capability for good vision both above and under water, and with preventing the aerial myopia. 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 just opposite to these narrow pupil holes. Both the pin‐hole pupils and low cornea curvature are devices to prevent aerial myopia. 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 versus aerial vision (see detail in Supin et al., 2001). A dolphin, when it looks at an underwater object, takes a position by the side to the object: it places the object of interest into a posterolateral part of the visual field, which projects onto the nasal area of high ganglion cell density. When a dolphin raises its head above the water surface to look at an above‐water object, it places the object in the ventronasal part of the visual field, which projects onto the temporal high‐resolution area of the retina (Dral, 1972, 1977; Dawson, 1980). 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 limited head mobility in many cetaceans. At low head mobility, even with 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.
Pinnipeds
Until recently, presence of high‐density areas in pinnipeds was considered questionable. Initial attempts to identify the area centralis in the retina of the California sea lion (Zalopus californianus) (Landau and Dawson, 1970), harp seal (Pagophilus groenlandicus) (Nagy and Ronald, 1970), and harbor seal (Phoca vitulina) (Jamieson and Fisher, 1971) did not reveal any areas of high ganglion cell density. Those authors studied transverse retinal sections. Later topographic mapping of ganglion cells in retinal whole‐mounts, however, revealed high‐density areas in five pinniped species belonging to different families, including Odobenidae: the walrus (Odobenus rosmarus) (Mass, 1992), Otariidae: northern fur seal (Callorhinus ursinus) (Mass and Supin, 1992) and Steller sea lion (Eumetopias jubatus) (Mass and Supin, 2005), and Phocidae: harp seal (Pagophilus groenlandicus) (Mass and Supin, 2003) and Weddell seal (Leptonychotes weddellii) (Welsch et al., 2001). Figure 10 presents typical examples of high‐ and low‐density areas in a whole‐mount of the harp seal's retina (Mass and Supin, 2003). It may be suggested that the presence of such an area is a characteristic of many, if not all, pinniped species. This area features a ganglion cell density that is many times higher than in the surrounding areas of the retina.

A,B: Microphotographs of the ganglion layer in a retinal whole‐mount of a harp seal: an area of high cell density (A) and an area of low cell density (B).
Topographic maps of ganglion cell density distribution of the northern fur seal (Callorhinus ursinus) and walrus (Odobenus rosmarus) are given in Figure 11A,B. In seals and sea lions, the area of increased ganglion cell density is located in the temporal retinal quadrant; it is of almost circular shape, strictly defined, and rather small, as compared with a very large total retinal surface (Fig. 11A). In this area, the peak cell density reaches 1,000–1,250 cells/mm2, and the density drops down sharply outside this region. The position of the high‐density area corresponds to the projection of the frontal visual field on the retina. This region belongs to the binocular sector of the visual field and provides the highest visual resolution and binocular vision.

A–D: Topographic distribution of ganglion cell density in the retina of some pinnipeds, the manatee and sea otter: the northern fur seal (A), the walrus (B), the manatee (C), and the sea otter (D). Designations as in Figure 9.
In terms of location on the retina, shape, and size, the area of high cell density is similar in both seals (Phocidae) and sea lions (Otariidae), specifically: the northern fur seal (Callorhinus ursinus) (Mass and Supin, 1992), harp seal (Pagophilus groenlandicus) (Mass and Supin, 2003), and Steller sea lion (Eumetopias jubatus) (Mass and Supin, 2005). The shape and position of the high‐density area in the retina indicates its close similarity to the area centralis of terrestrial carnivores (Stone, 1983; Peichl, 1992; Williams et al., 1993). The cell density in this area of all studied pinnipeds (1,000–2,500 cells/mm2) is several times lower than that in some terrestrial carnivores: for example, approximately 7,000–10,000 cells/mm2 in the domestic cat (Stone, 1983; Wong and Hughes, 1987; Williams et al., 1993), and up to 6,000–14,000 cells/mm2 in the dog and wolf (Peichl, 1992). However, because of the much larger size of the eyeball in pinnipeds, the cell density per angular unit of the visual field is of the same order as in terrestrial carnivores, 200–400 cells/deg2.
The retinal topography is substantially different in a representative of another pinniped family, Odobenidae—the walrus (Odobenus rosmarus) (Fig. 11B) (Mass, 1992). The area of increased ganglion cell density is not defined as clearly as in otariides and phocides. It appears as a horizontally extended oval, resembling the visual streak of terrestrial mammals. Within this streak, the highest cell density in its temporal part exceeds 1,000 cells/mm2; because of smaller size of the walrus eye, this cell density does not exceed 50 cells/deg2.
Sirenians
The topographic organization of the retinal ganglion layer was studied by Mass et al. (1997) in the Florida manatee (Trichechus manatus latirostris) using the Nissl‐stained retinal whole‐mount technique. It appeared that ganglion cell distribution was not uniform, but varied smoothly across the retina. The pattern of ganglion cell distribution is presented in Figure 11C. This pattern of distribution can be described as bell‐shaped—that is, cell density was higher in a large part around the center of the retina (except far periphery), and the highest cell density was located below the optic disk. The cell density in this region exceeded 250 cells/mm2. For a rather small manatee eye, this corresponds to 6–7 cells/deg2. Thus, there is no clearly restricted area of high cell density similar to the area centralis or visual streak of terrestrial mammals. This type of ganglion cell distribution may be considered as an example of low specialization.
Sea Otters
In the retina of the sea otter (Enhydra lutris), ganglion cells topography (Fig. 11D) has several features similar to that of terrestrial mammals (Mass and Supin, 2000). The high‐density area appears as a nasotemporal streak. Within the temporal part of this streak, 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 approaches 4,000 cells/mm2; in a rather small eye of the sea otter, this corresponds to 50–60 cells/deg2.
CONCLUSION
In general, the visual system of marine mammals demonstrates a rather high degree of development and also several specific features associated with adaptation to both aquatic and aerial environment. In particular, adaptation is seen in the marine mammal eye to low‐luminosity conditions, specific retinal topography (positions of high cell density indicating best‐vision areas), along with structural adaptations of the pupil and cornea that provide emmetropia both in air and water.
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