Adaptive Features of Aquatic

Mammals Eye
ALLA M. MASS* AND ALEXANDER YA. SUPIN
Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences,
Moscow, Russia
ABSTRACT
The eye of aquatic mammals demonstrates several adaptations to
both underwater and aerial vision. This study offers a review of eye anat-
omy 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 myo-
pia. As underwater vision necessitates adjusting to wide variations in lu-
minosity, iris muscle contractions create species-specic pupil shapes that
regulate the amount of light entering the pupil and, in pinnipeds, work
in conjunction with a reective optic tapetum. The retina of aquatic mam-
mals is similar to that of nocturnal terrestrial mammals in containing
mainly rod photoreceptors and a minor number of cones (however, resid-
ual 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 concentra-
tion (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 de-
velopment and several specic features associated with adaptation for
vision in both the aquatic and aerial environments. Anat Rec 290:701
715, 2007. 2007 Wiley-Liss, Inc.
Key words: vision; ocular optics; retina; ganglion cells; retinal
topography; aquatic mammals
Comparative studies of the visual system in animals
adapted to various living conditions have revealed new
specic 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), sire-
nians (manatees and dugongs), and sea otters. These spe-
cies demonstrate various extents of adaptation to the
aquatic environment. Many aquatic mammals (cetaceans,
sirenians) spend their entire life in the water; however,
air-breathing connes them to a near-surface layer of
water. Other marine mammals (pinnipeds, sea otters)
spend a signicant part of their life on land. As a result,
the visual systems of these groups feature remarkable
morphological and functional specializations for both
*Correspondence to: Alla M. Mass, Severtsov Institute of
Ecology and Evolution, Russian Academy of Sciences, 33 Lenin-
sky Prospect, 119071 Moscow, Russia.
E-mail: alla_mass@sevin.ru
Grant sponsor: The Russian President; Grant number: NSh-
7117.2006.4; Grant sponsor: The Russian Foundation for Basic
research; Grant numbers: 04-04-48137 and 07-04-00098.
Received 2 March 2007; Accepted 6 March 2007
DOI 10.1002/ar.20529
Published online in Wiley InterScience (www.interscience.wiley.
com).
2007 WILEY-LISS, INC.
THE ANATOMICAL RECORD 290:701715 (2007)
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 struc-
tures of the eye in cetaceans are determined primarily by
the optical properties of the aquatic medium and by sev-
eral 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 signicantly differ-
ent from those in terrestrial mammals.
Characteristic examples of eye structure in cetaceans
are presented in Figure 1AD. Prominent features typical
for all cetaceans are a thick sclera (particularly so in
baleen whales, or mysticetes, Fig. 1C), a signicantly
thickened cornea, a highly developed choroid, a highly
developed vascular network forming a typical rete mira-
bilia that lls a signicant 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.
The shape of the eyeball is markedly altered as com-
pared with terrestrial mammals. While the eyecup in ter-
restrial mammals is typically almost spherical, there is
substantial attening of the anterior segment in ceta-
ceans. As a result, the axial length of the eyecup is much
smaller than its diameter. As a rst approximation, the
eyecup shape is close to a hemisphere. More precisely
speaking, the shape approximates not a complete hemi-
sphere, but a segment of a sphere of a large arc of approx-
imately 150 degrees, as delimited by arrows in Figure
1AC.
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 nding is characteristic of
both odontocetes (toothed whales) and mysticetes (baleen
whales) (Pu tter, 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 (Del-
phinapterus 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 refrac-
tion in the cetacean eye is not as crucial as in terrestrial
mammals, it does contribute to refraction. The outer cor-
neal surface has lower curvature than the inner surface
(Kroger 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 61 diopters under water (Kroger and Kirsch-
feld, 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; Kroger and
Fig. 1. AD: 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.
702 MASS AND SUPIN
Kirschfeld, 1994). Nevertheless, this refractive index is
little different from that of water (1.331.34). 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 mys-
ticetes and the beluga whale, of a slightly elliptical shape
(see Fig. 1). The curvature of the lens surface provides
sufcient 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 sh, thus reecting the common environmen-
tal constraints of the optical properties of water.
A strongly convex (spherical) lens consisting of homoge-
neous 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 re-
fractive index than the inner core (Rivamonte, 1976; Kro-
ger 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 signicantly 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
mammalsthat is, change of the lens shape by the ciliary
muscle. The ciliary muscle is poorly developed in all dol-
phins and is absent from most whales (Waller, 1984; West
et al., 1991; Bjerager et al., 2003), suggesting that accom-
modation cannot be achieved by a change of the lens
shape (Dral, 1972). This suggestion is supported by oph-
thalmoscopic observations (Dawson et al., 1987b), which
revealed no signicant accommodative changes. It has,
however, been suggested that accommodation in ceta-
ceans does occur by another mechanism, namely, by axial
displacement of the lens due to changes in intraocular
pressure. Intraocular pressure can change because of con-
traction 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 pres-
sure decreases thus shifting the lens backward (Kroger
and Kirschfeld, 1989).
Adaptation of the cetacean eye to underwater vision is
also evident in the structure of the iris and pupil. Ceta-
cean 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 illu-
minations 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 con-
tracted (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 illumina-
tion, 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 del-
phis), tucuxi (Sotalia uviatilis), 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 char-
acteristic 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 ter-
restrial mammals.
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 refrac-
tive power of the most convex central part of the corneal
surface by approximately 20 diopters (Dral, 1972; Daw-
son 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 attened
(low-curvature) regions of the cornea. Keratoscopic stud-
ies 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 (Riva-
monte, 1976). An additional correction for aerial myopia
Fig. 2. AC: Shape of the pupil in the bottlenose dolphin at various levels of illumination: low illumina-
tion, nonconstricted oval pupil (A); moderate illumination, partially constricted U-shaped pupil (B); high
illumination, strongly constricted pupil reduced to two pinholes (C).
703 ADAPTIVE FEATURES OF AQUATIC MAMMALS EYE
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 reective layer, the
tapetum lucidum. The tapetum is present in all ceta-
ceans, 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 brils (tapetum brosum).
Multiple reection of light from 5070 layers of brils
results in signicant light reection 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 ta-
petum does not usually extend below the horizontal equa-
tor 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 dif-
ference from cetaceans, has some common features
reecting 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 equi-
distant from the lens center. Thus, the eye optics, as in
cetaceans, is almost centrally symmetrical.
The iris in pinnipeds is very muscular and heavily vas-
cularized. The dilatator muscle is well developed. Most
pinnipeds have a pupil that becomes pear-shaped when
constricted. An exception is the diagonal pupil in Erigna-
thus 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 pupil-
Fig. 3. AD: 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, attened 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.
704 MASS AND SUPIN
lary area variation is rather small: 70.5 times in the har-
bor seal (Phoca vitulina), and 26 times in the California
sea lion (Zalophus californianus). In a deep diver, the
northern elephant seal (Mirounga angustirostris), the pu-
pil area varied within an extremely wide range, from a
giant area of 422 mm
2
in dark-adapted conditions
(approximately 23 mm in diameter) to a pinhole opening
of 0.9 mm
2
in light-adapted conditions, that is, the range
of variation is almost 470 times (Levenson and Schuster-
man, 1997).
The ciliary muscle in pinnipeds is much better devel-
oped 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 pin-
nipeds, both otariids and phocids, has a clearly delimited
region (610 mm in diameter) of almost at surface. It is
located near the center of the cornea (FC region in Fig.
3A). The at region of the cornea serves as an emmetropic
window in which refraction remains almost equal both
in water and air. The presence of this at region was
demonstrated by precise measurements in the Califor-
nian sea lion (Dawson et al., 1987b). In another pinniped,
the hooded seal (Cystophora cristata), the attened 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 attened 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 pres-
sure in pinnipeds are absent, but the at 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 devel-
oped reective 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 re-
ective rodlets (tapetum cellulosum) (Braekevelt, 1986).
It consists of 20 to 34 layers, and covers a large propor-
tion of the fundus (Nagy and Ronald, 1970, 1975; Jamie-
son 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 sub-
species of the West Indian manatee) by Mass et al. (1997).
In both T. manatus and T. inunguis, the eye is rather
small (1319 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 dif-
fers 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 cur-
vature 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 manatees vision. The sclera is thin.
Thus, despite a completely aquatic mode of life, the eye
anatomy of the manatee retains several conservative fea-
tures. 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 Muste-
lidae family, represents an example of transition of ter-
restrial 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 mam-
mals: it is almost spherical, axial length is only a little
shorter than the diameter. Contrary to spherical lenses of
cetaceans and pinnipeds, the sea otters 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 sur-
face. Therefore, contraction of iris muscles inuences 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 refrac-
tion 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), Dalls porpoise (Phocenoides dalli) (Murayama
et al., 1992a, 1995), beluga (Delphinapterus leucas)
(Pu tter, 1903; Pilleri, 1964), pilot whale (Globicephala
melaena) (Peichl et al., 2001), n whale (Balaenoptera
physalus) (Pilleri and Wandeler, 1964), and minke whale
(B. acutorostrata) (Murayama et al., 1992a,b). The lami-
nar structure of the retina in all cetaceans is qualitatively
similar to that in terrestrial mammals (Fig. 4A,B). It con-
sists of the receptor layer, outer nuclear layer, outer plexi-
form layer, inner nuclear layer, inner plexiform layer,
705 ADAPTIVE FEATURES OF AQUATIC MAMMALS EYE
ganglion cell layer, and, nally, the optic-ber 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 lami-
nar structure of the retina shows no radical changes and
contains all the layers (Dral and Beumer, 1974; Purves
and Pilleri, 1974).
Although qualitatively similar to other mammals, the
laminar structure of the retina in cetaceans markedly dif-
fers quantitatively. The cetacean retina is much thicker
than that of terrestrial mammals, reaching up to 425 mm
(Dral, 1977; Dawson et al., 1982; Murayama et al., 1995).
For comparison, the thickness of the retina in diurnal ter-
restrial mammals is 110220 mm (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 rst 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 proles in the receptor
layer and different sizes of photoreceptor endings in the
outer plexiform layer, which are indicative of different re-
ceptor 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 Dalls porpoise (Phocoenoides
dalli) (Murayama et al., 1995) and pilot whale (Globice-
phala melaena) (Peichl et al., 2001). Two types of recep-
tors 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 trunca-
tus) (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 pro-
portion is in the range of 1% (Peichl et al., 2001). The cone
density observed in marine mammals (3,0007,000/mm
2
up to 10,000/mm
2
in the harbor porpoise, Phocoena pho-
coena) is close to that of nocturnal terrestrial mammals
(2,2007,000/mm
2
, 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 conrming
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 nu-
clear layer, the outer plexiform layer, the inner nuclear
layer, and the inner plexiform layer, based on Golgi prep-
arations 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, ama-
crine, 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 ceta-
ceans 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 sepa-
rated by wide intercellular spaces. This cell pattern was
described in Nissl-stained retinal transverse sections
from the beluga whale (Delphinapterus leucas) (Pu tter,
1903; Pilleri, 1964), n whale (Balaenoptera physalus)
(Pilleri and Wandeler, 1964), and Dalls porpoise (Phocoe-
Fig. 4. 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 nu-
clear layer; IPL, inner plexiform layer; GL, ganglion cell layer. Giant
ganglion cells are visible in the ganglion layer.
706 MASS AND SUPIN
noides 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) (Mur-
ayama 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 mm in diameter, and light nucleolus of
4 to 5 mm in diameter. Cell bodies contained easily visible,
intensely stained Nissl granules. All large neurons (par-
ticularly giant neurons of the whale retina) showed sev-
eral axon/dendrite bases.
A remarkable feature of the cetacean retina is the pres-
ence of extremely large, giant ganglion cells. Most gan-
glion cells in the cetacean retina are of rather large size,
but giant cells reach 5080 mm and more. These large
neurons have been described in many studies of several
dolphin species: in the bottlenose dolphin (Tursiops trun-
catus) (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), Dalls porpoise (Phocoenoides dalli) (Mur-
ayama et al., 1995), Chinese river dolphin or baiji (Lipotes
vexillifer), and nless porpoise (Neophocaena phocae-
noides) (Gao and Zhou, 1987), and in a few mysticete spe-
cies (Pilleri and Wandeler, 1964; Murayama et al.,
1992a,b; Mass and Supin, 1997).
It should be noted that the term giant as applied to ter-
restrial mammals suggests a ganglion cell size between
1535 mm, 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 mm.
In some cetacean species, ganglion cells do not reach
such large sizes. In the Amazon river dolphin (Inia geof-
frensis), the largest ganglion cells do not exceed 40
42 mm (Waller, 1982; Mass and Supin, 1989); in the retina
of the Ganges river dolphin (Platanista gangetica), gan-
glion cells larger than 20 mm were not found (Dral and
Beumer, 1974). However, even these cells are markedly
larger than ganglion cells in many terrestrial mammals.
Fig. 5. AD: 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).
707 ADAPTIVE FEATURES OF AQUATIC MAMMALS EYE
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 bottle-
nosed dolphin (Tursiops truncatus) (Fig. 5A,B), gray
whale (Eschrichtius robustus) (Fig. 5C,D), and tucuxi dol-
phin (Sotalia uviatilis) (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 mm, although cells
as large as 5060 mm are also present, and there are no
cells smaller than 812 mm. Large cells, over 35 mm, 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 mm or more, is also characteristic of reti-
nas of other cetacean species: the harbor porpoise (Pho-
coena phocoena) (Mass and Supin, 1986), Amazon river
dolphin (Inia geoffrensis) (Mass and Supin, 1989), minke
whale (Balaenoptera acutorostrata) (Murayama et al.,
1992a,b), and Dalls porpoise (Phocoenoides dalli) (Mur-
ayama et al., 1995).
The size histograms of cetaceans ganglion cells are
monomodal; however, the tail represents cells larger
than 4045 mm. This tail contains a small part of the total
cell population. For example, in the bottlenose dolphin
(Tursiops truncatus), cells larger than 40 mm 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 (Delphi-
napterus 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 dol-
phin (Sotalia uviatilis), the largest cells (3659 mm) 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 mm (giant) cells (Mass and Supin,
1999). In the Chinese river dolphin or baiji (Lipotes vexil-
lifer), the ganglion cell sizes were reported as distributed
in a bimodal manner with peaks at 13 and 40 mm (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 2530 mm (Hebel and Hol-
lander, 1979; Stone and Halasz, 1989).
Pinnipeds
Laminar organization of the retina in pinnipeds (Fig.
6A,B) generally corresponds to that of terrestrial mam-
mals (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.
As in terrestrial carnivores with nocturnal vision, the
receptor layer of the retina in all pinnipeds thus far stud-
ied 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 thick-
est 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
ve 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/mm
2
up to 10,000/mm
2
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 sensi-
tive S-opsin. This feature is common in cetaceans (despite
Fig. 6. 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).
708 MASS AND SUPIN
the very different phylogenies of cetaceans and pinni-
peds), 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 dif-
fusely distributed. Only slight ordering can be seen near
the outer and inner plexiform layers. This nding con-
trasts 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 distrib-
uted 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 laments.
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 mm with a separate group of giant cells larger than
3540 mm (Fig. 7AD). In the northern fur seal (Callor-
hinus ursinus), ganglion cells are mostly of 14 to 28 mm
with the largest cells up to 50 mm (Mass and Supin,
1992); in the Steller sea lion (Eumetopias jubatus), the
majority of cells are 10 to 25 mm with some cells are as
large as 37 mm (Mass and Supin, 2005); in the harp seal
(Pagophilus groenlandicus), typical cells are 20 to 30 mm
with some cells were as large as 60 mm (Nagy and Ronald,
1970; Mass and Supin, 2003). Giant ganglion cells were
noticed also in the retina of the harbor seal (Phoca vitu-
lina) (Jamieson and Fisher, 1971). The percentage of
giant cells (810% in the northern fur seal, 56% in the
harp seal, 8% in the Steller sea lion) is close to corre-
sponding proportions of a-cells described in other mam-
mals: from 1 to 10% (Peichl, 1991). The similarity of giant
Fig. 7. AD: 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).
709 ADAPTIVE FEATURES OF AQUATIC MAMMALS EYE
cells in pinnipeds to ganglion a-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 2530 mm (Fukuda
and Stone, 1974; Hughes, 1981; Wong and Hughes, 1987).
Sirenians
Data on retinal organization of sirenians are rare. The
rst description of the manatees retina was published
by Pu tter (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 manatees 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 func-
tioning well in both air and water.
Contrary to aquatic and similarly to terrestrial mam-
mals, majority of ganglion cells in the sea otters retina
are rather small, of 8 to 18 mm, mostly 1115 mm in the
retinal area of high ganglion cell density, up to 28 mm in
the peripheral area of low cell density (Fig. 7E,F); only
6% of cells are larger than 30 mm (Mass and Supin, 2000).
Mean cell size in the high-density streak in the sea otters
retina (1115 mm) is also close to that of terrestrial mam-
mals. In the retinal periphery, cell size distribution
reveals three distinctive size groups: 818, 1728, and
2947 mm (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 a-, b-, and g-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 den-
sity. Mammals with frontal vision have a fovea, or area
centralis, located in the center of the visual eld. This ret-
inal 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 hori-
zontal 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 mam-
mals 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 (at mounts)
became used for investigation of distribution of ganglion
cells. Several cetacean species were investigated using
the retinal whole-mount method, mostly marine odonto-
cetes: the common dolphin (Delphinus delphis) (Dral,
1983), bottlenose dolphin (Tursiops truncatus) (Dral,
Fig. 8. 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).
710 MASS AND SUPIN
1975a, 1977; Mass and Supin, 1995), harbor porpoise
(Phocoena phocoena) (Mass and Supin, 1986), Dalls por-
poise (Phocoenoides dalli) (Murayama et al., 1995), tucuxi
dolphin (Sotalia uviatilis) (Mass and Supin, 1999), pa-
cic white-sided dolphin (Lagenorhynchus obliquidens)
(Murayama and Somiya, 1998), and beluga whale (Del-
phinapterus 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).
The most characteristic feature of all these dolphin spe-
cies 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. 9AC). 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 trun-
catus), both these areas are located at a distance of 1516
mm from the optic disk, which corresponds to 5055
degrees of the visual eld. Ganglion cell density is almost
equal in each of these areas. It reaches 700800 cells/
mm
2
(Fig. 9A), which corresponds to 4050 cells per
squared degree of the visual eld (cells/deg
2
). 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 and porpoise species, the retinal topog-
raphy is generally similar to that described above for Tur-
siops 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
eld) is higher than in the nasal region. Species with this
morphology include: the harbor porpoise (Phocoena pho-
coena) (Mass and Supin, 1986), Dalls porpoise (Phocoe-
noides 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, gan-
glion cell density varies quantitatively between species.
For example, in the riverine tucuxi (Sotalia uviatilis),
the ganglion cell density does not exceed 200 cells/mm
2
(Fig. 9B); in the small tucuxi eyeball, this value corre-
sponds to a rather low density per squared degree, not
more than 56 cells/deg
2
(Mass and Supin, 1999).
Retinal topography of ganglion cells was also studied in
two mysticete species: the gray whale (Eschrichtius gib-
bosus) (Mass and Supin, 1997) and minke whale (Balae-
noptera 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 sec-
Fig. 9. AD: 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 mm
2
and is shown by var-
ious 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, re-
spectively.
711 ADAPTIVE FEATURES OF AQUATIC MAMMALS EYE
tors. Note that ganglion cell density in the grey whale (up
to 200 cells/mm
2
, 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/deg
2
. 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 fea-
ture of many cetaceans, both odontocetes and mysticetes.
The Amazon river dolphin (Inia geoffrensis) presents a
specic 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 ter-
restrial mammals, this area is located not in the central
part of the retina, but in the ventral partthat is, in the
region responsible for the upper portion of the visual eld
(Mass and Supin, 1989). The density of ganglion cells
in the high-density area of the Amazon river dolphin
reaches 400500 cells/mm
2
; with the small size of the eye-
ball, this value corresponds to a density of less than 3
cells/deg
2
when projected onto the visual eld.
A question arises whether the difference between ma-
rine cetaceans (marine dolphins and whales) and the
Amazon river dolphin in their retinal topography is asso-
ciated with their different systematic position (the Ama-
zon 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
uviatilis) (Mass and Supin, 1999), nless porpoise (Neo-
phocoena 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 specic organiza-
tion 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 signicance of this mode of ret-
inal organization. The presence of the two areas of high
ganglion cell density (i.e., of high retinal resolution) may
be associated with the cetaceans 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 curva-
ture 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 pro-
jected 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 posterolat-
eral part of the visual eld, 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 eld, 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 eld, which is very
important for forward-moving animals. The existence of
two high-resolution areas of the retina can also compen-
sate for limited head mobility in many cetaceans. At low
head mobility, even with high mobility of the eyes, a sin-
gle 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 pinni-
peds was considered questionable. Initial attempts to iden-
tify 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 ve
pinniped species belonging to different families, including
Fig. 10. 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).
712 MASS AND SUPIN
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 seals ret-
ina (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 den-
sity that is many times higher than in the surrounding
areas of the retina.
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 cir-
cular shape, strictly dened, and rather small, as compared
with a very large total retinal surface (Fig. 11A). In this
area, the peak cell density reaches 1,0001,250 cells/mm
2
,
and the density drops down sharply outside this region.
The position of the high-density area corresponds to the
projection of the frontal visual eld on the retina. This
region belongs to the binocular sector of the visual eld and
provides the highest visual resolution and binocular vision.
In terms of location on the retina, shape, and size, the
area of high cell density is similar in both seals (Pho-
cidae) and sea lions (Otariidae), specically: 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/mm
2
) is several times lower than that in
some terrestrial carnivores: for example, approximately
7,00010,000 cells/mm
2
in the domestic cat (Stone, 1983;
Wong and Hughes, 1987; Williams et al., 1993), and up to
6,00014,000 cells/mm
2
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
eld is of the same order as in terrestrial carnivores, 200
400 cells/deg
2
.
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 dened
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/mm
2
;
because of smaller size of the walrus eye, this cell density
does not exceed 50 cells/deg
2
.
Fig. 11. AD: 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.
713 ADAPTIVE FEATURES OF AQUATIC MAMMALS EYE
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-shapedthat is, cell
density was higher in a large part around the center of
the retina (except far periphery), and the highest cell den-
sity was located below the optic disk. The cell density in
this region exceeded 250 cells/mm
2
. For a rather small
manatee eye, this corresponds to 67 cells/deg
2
. Thus,
there is no clearly restricted area of high cell density sim-
ilar 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-dened 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/mm
2
; in a rather small eye of the sea otter,
this corresponds to 5060 cells/deg
2
.
CONCLUSION
In general, the visual system of marine mammals dem-
onstrates a rather high degree of development and also
several specic features associated with adaptation to
both aquatic and aerial environment. In particular, adap-
tation is seen in the marine mammal eye to low-luminos-
ity conditions, specic retinal topography (positions of
high cell density indicating best-vision areas), along with
structural adaptations of the pupil and cornea that pro-
vide emmetropia both in air and water.
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Cohen JL, Tucker GS, Odell DK. 1982. The photoreceptors of the
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