Download Color Vision in Marine Mammals: A Review

Bright, M., P.C. Dworschak & M. Stachowitsch (Eds.) 2002: The Vienna School of
Marine Biology: A Tribute to Jörg Ott. Facultas Universitätsverlag, Wien: 73-87
Color Vision in Marine Mammals:
A Review
Ulrike Griebel
Konrad Lorenz Institute for Evolution and Cogition Research, Adolf Lorenz Gasse 2, A3422, Altenberg, Austria. E-mail: [email protected]
Keywords: marine mammals, dolphins, seals, manatees, color vision
Abstract. Marine mammals present a unique opportunity to study the course of
evolutionary development of visual processes in their adaptation from a terrestrial
to an underwater environment. The ambient light conditions in the oceans differ
considerably from those on land and pose different challenges to the visual system. The optic mechanisms and the retinal structures of the eyes of marine mammals show specific adaptations for vision in both media. The present review delineates the environmental conditions of life in the ocean that have shaped the color
vision systems in the various marine mammals.
Recent findings have shown that cetaceans and pinnipeds have a very unusual
visual system among the mammals because they seem to have lost their short-wavelength-cones completely. Nevertheless, behavioral data indicate that all three groups
of marine mammals discussed here (cetaceans, pinnipeds, and manatees) are able
to discriminate colors. A possible underlying mechanism for color vision in pinnipeds and cetaceans could be based on the comparison of rod and cone signals.
Introduction
The ambient light conditions in the oceans differ considerably from those on land
and pose different challenges to the visual system. Marine mammals offer an
excellent opportunity to study the evolutionary changes of visual systems in their
adaptation from a terrestrial to an underwater environment. The evolution of vertebrate eyes actually started in water. Quite early in the history of vertebrates,
there were fish with well-developed eyes. These eyes were passed via amphibians
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and reptiles to birds and mammals, while being greatly modified to function in air.
When representatives from various vertebrate classes returned to the water, their
eyes had to become "fishlike" again in many respects.
Marine mammals like whales and dolphins, seals, and sea cows vary in the
extent of their adaptation to the aquatic environment. Dolphins, whales, and sea
cows spend all their life in water, whereas pinnipeds are amphibious and divide
their time between land and sea. Interestingly, not only the amphibious seals but
also the whales and dolphins can see well in air. The optic mechanisms and the
retinal structures of the eyes of marine mammals show specific adaptations for
vision in both media; this is – with some exceptions – very unlike the situation in
fish and indicates functional and anatomical differences.
The various groups of marine mammals - dolphins and whales, seals, and manatees - have developed from different terrestrial ancestors. The present review
delineates the environmental conditions of life in the ocean that have shaped the
color vision systems in all these groups.
The term "color vision" refers to the capability of a visual system to respond differently to light differing in wavelength only. It is based on the existence of two
or more photoreceptor types containing photopigments that maximally absorbe in
different spectral ranges. The processing of color-specific information in the eye
and brain gives rise to the perception of color as a subjective phenomenon. We
classify colors in terms of "hue", "brightness" and "saturation", and name different hues with the basic color terms "blue, green, yellow, red" as well as "white"
and "black". But human color vision is only one realization of color vision in the
animal kingdom. Most mammals are dichromats, which means that they have two
cone types, one maximally sensitive in the long or middle wavelength range of the
spectrum (L-cone, green- to red-sensitive, depending on species) and one maximally sensitive in the short wavelength range (S-cone, blue- to UV-sensitive,
depending on species) (Jacobs, 1993; Ahnelt & Kolb, 2000). In primates alone,
including humans, three cone types (yielding 'trichromacy') have evolved by
duplication of the L-opsin gene. As a result primates have red and green cones in
addition to blue cones (Jacobs, 1993; Nathans, 1999). Monochromacy, the possession of one cone type only and thus the absence of cone-based color vision, is
rare among mammals and is found in only a few nocturnal species (Jacobs, 1993;
Ahnelt & Kolb, 2000). Hence, dichromacy seems to be the rule across mammals,
and could also be expected in marine mammals, which all have daylight activity
phases and apparently use aerial vision on a regular basis.
Interestingly and unexpectedly, however, it seems that at least two groups of
marine mammals, the pinnipeds and the cetaceans, have lost their S-cones in the
evolutionary process of adapting to the marine environment (Crognale et al.,
1998; Fasick et al., 1998; Peichl & Mountairou, 1998; Peichl et al., 2001).
Color vision in marine mammals
75
Cetacea
The cetacean eye has faced several environmental challenges in the course of evolution. It had to be re-adapted to the mechanical, chemical, osmotic and optical
conditions of the aquatic medium. There is no doubt that dolphins are highly auditory animals and use echolocation extensively in their natural habitat. Their auditory capabilities and mechanisms have been studied in detail, while their visual
capacities are poorly understood and often underrated. Dolphin vision serves many
important biological functions such as prey detection and capture, conspecific and
individual identification, and migration and orientation. A blindfolded dolphin
may have difficulty finding fish at very close range even while echolocating. Also
their performance in air suggests well developed visual function. Numerous learning experiments have demonstrated that the dolphin's visual system also supports
important cognitive functions like conceptualization and communication.
The cetacean eye has clearly been modified for high sensitivity by virtue of its
complete retinal tapetalization, its large cornea, and its large pupillary opening
that can be constricted drastically in bright light conditions above the water
(Dawson, 1980). The retina of cetaceans has rods and cones (RochonDuvigneaud, 1940; Mann, 1946; Pilleri, 1964, 1967; Pilleri & Wandeler, 1964;
Peers, 1971; Dawson & Perez, 1973; Andreyev, 1974; van Esch & de Wolf, 1979;
Dawson, 1980; Kastelein et al., 1990). The retina is extremely rod dominated, but,
according to reports on several species, the distribution and frequency of receptor
types varies (Pütter, 1903; Pilleri & Wandeler, 1970; Perez et al., 1972; Dral,
1977; Peichl & Behrmann, 1999; Peichl et al., 2001).
The ganglion cells of the retina are divided into several morphologically different types (Dral 1977, 1983; Mass et al., 1986; Mass & Supin, 1990; Gao & Zhou,
1987; Murayama et al., 1992; Murayama et al., 1995, Li et al., 1986) and are not
evenly distributed over the retina. In the species examined so far, two regions of
maximum cell density lie relatively far from the optical axis in the rostroventral
and caudodorsal areas of the intermediate retina (Dral, 1977, 1983; Mass & Supin,
1986, 1995, 1997). The temporal area is probably used for frontal, binocular
vision and the nasal zone for panoramic vision.
The rod pigments of whales are rhodopsins (based on retinal-1) as in other
mammals, but show a broader spectral tuning curve than do those of terrestrial
mammals (McFarland, 1971; Fasick & Robinson, 2000). The underwater light
field becomes successively blue-shifted with depth, and the distribution of the rod
absorption maxima indicates an adaptation to the dominant wavelengths in the
environment of the species, similar to the λmax ranges in many deep-sea fishes.
Rod absorption maxima range from 481 nm in the deep-diving Baird's Beaked
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Whale (Berardius bairdi), to 486 nm in bottlenose dolphin, a species that is pelagic but hunts in coastal waters, to 496 nm in the grey whale (Eschrichtius robustus), a species that bottom feeds and lives in shallow neritic waters.
In recent studies (Fasick et al., 1998; Fasick & Robinson, 1998, 2000) the opsin
genes of the bottlenose dolphin were cloned and expressed. A rod and a longwavelength sensitive (L) cone opsin cDNAs were identified. The resulting pigments had absorption maxima (λmax) of 488 nm for the rod and 524 nm for the
cone. A gene which coded for a short-wavelength sensitive cone opsin (S-opsin)
was also found, but it contained a deleterious mutation that prohibited the expression of the S-opsin protein. Another recent study using immunocytochemistry
confirmed the loss of the S-cones for seven species of toothed whales (including
the bottlenose dolphin) and, interestingly, also for a number of pinniped species
(Peichl et al., 2001). The data suggest that dolphins and whales should lack the
dichromatic form of color vision typical of most terrestrial mammals.
To date, electrophysiological studies on spectral sensitivity and color vision are
nonexistent and behavioral investigations are extremely rare due to problems in
availability of animals for these experiments and also because of the long duration of such studies. The only way to demonstrate that an animal actually uses
color information is to perform behavioral experiments. The most appropriate
method in mammals is a training technique in which the animals are rewarded
with food. In a general test to establish the presence of color vision the evidence
is given by demonstrating that the animal uses only the "color" cue, and not
"brightness", to discriminate between the different stimuli.
The first behavioral study on color vision was done by Madsen (Madsen, 1976;
Madsen & Herman, 1980) with a bottlenose dolphin (Tursiops truncatus). The
animal had to discriminate a colored light from a white light and also two colored
lights (the stimuli were varied in intensity), first in a go-no go discrimination task,
and then in a successive two-choice discrimination task with one stimulus field
and two response paddles. In both protocols the color stimuli were used as cues
in a spatial reversal problem. Under these conditions the experimental dolphin did
not demonstrate color discrimination.
Madsen calculated the spectral sensitivity curve based on a brightness match
between a red, a green, and a blue monochromatic light. Under photopic conditions
the dolphin’s spectral sensitivity function peaked at 500 nm and shifted to 496 nm
under scotopic conditions. The shift is not very large, but conditions could have
been only mesopic for the dolphin, since the experiment was conducted under the
night sky. This result indicates a rod and a green cone mechanism. The data indicate
a shift of 10 nm more toward the longer wavelengths than would be expected, based
on the maximum photopigment absorption point (486 nm) reported for the extract-
Color vision in marine mammals
77
ed rod pigments of Tursiops by McFarland (1971). On the other hand, behaviorally
or electrophysiologically measured sensitivity curves often show a shift the absorption maxima of the respective pigments because of in screening and other effects.
A recent study re-examined dolphin spectral sensitivity behaviorally (Griebel &
Schmid, in press). Here, spectral sensitivity was measured in air with a lightadapted bottlenose dolphin in a spectral range from 397 nm to 636 nm in a simultaneous two-choice discrimination test by determining increment thresholds. The
resulting spectral sensitivity curve was very broad, suggesting the contribution of
more than one pigment maximum sensitivity occurred in the blue-green part of the
spectrum at about 490 nm. Since dolphins have lost their S-cones, the second pigment contributing to the spectral sensitivity function is probably the rod pigment.
Interestingly, the curve rose again in the near UV, suggesting a second maximum
here. Two wavelength discrimination tasks where brightness was adjusted to the
dolphin's subjective spectral sensitivity showed that the animal could discriminate
between 397nm and 487nm, but not between 457nm and 544nm. This result suggests that a mechanism for color discrimination is present even in the absence of
S-cones.
Pinnipedia
Unlike the cetaceans and manatees, pinnipeds are amphibious and spend a substantial portion of their time on land for resting, giving birth, mating, and moulting. Like cetaceans, many pinnipeds also experience low light intensities when
diving or foraging at night. They did not evolve echolocation, but possess very
sensitive vibrissae which they use for turbulence tracking (Dehnhardt et al.,
1998). As indicated by their big eyes, vision plays a significant role in pinnipeds
for various biological functions like hunting, orientation, and communication.
Like other mammals which live in low light conditions, the retinas of pinnipeds
have well developed tapeta (Braekevelt, 1986a) and are densely populated with
highly light-sensitive rods (Landau & Dawson, 1970; Jamieson & Fisher, 1971;
Nagy & Ronald,1975; Andreev et al., 1975; Mass, 1992; Peichl et al., 2001).
Histological studies using both light and electron microscopy revealed cone-like
receptors in the eyes of several species of pinnipeds (Jamieson & Fisher, 1971;
Nagy & Ronald, 1975; Peichl & Moutairou, 1998; Peichl et al., 2001). There is
also some psychophysical evidence for a duplex retina for P. groenlandicus and
Mirounga angustirostris. The duplex retina is suggested by a Purkinje shift, by a
break in the dark adaption curve (Lavigne & Ronald, 1972; Levenson, 1997;
Levenson & Schusterman, 1998), and by a break in the critical flicker frequency
curve (Bernholz & Matthews, 1975).
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The rod pigments of pinnipeds are shifted in sensitivity towards light of shorter wavelengths than those of most terrestrial mammals (Lythgoe & Dartnal, 1970;
Lavigne & Ronald, 1975; Carlson & LeBoeuf, 1998; Fasick & Robinson, 2000),
usually with a peak sensitivity at about 496 nm, which is also the case for the shallow-diving California sea lion and harbor seal. The deep-diving northern elephant
seal has a rod pigment with an even greater blue-shift in sensitivity to 486 nm
(Lythgoe & Dartnall, 1970; Carlson & LeBoeuf, 1998). Furthermore, the rod system in this species seems to be able to adapt extremely fast, attaining its threshold
sensitivity within 6 minutes (Levenson & Schusterman, 1999).
Behavioral measurement of photopic spectral sensitivity showed that maximum
spectral sensitivity for the harp seal was at 550 nm (Lavigne & Ronald, 1972).
Another behavioral study of photopic spectral sensitivity in the harbor seal and
Southern sea lion yielded similar results (Griebel & Schmid, submitted); the former
had a peak sensitivity around 500 nm, the latter around 540 nm. In both of these
studies the main peak was very broad, suggesting the contribution of a second pigment type (probably the rod pigment), and, interestingly, all these behavioral
curves have a smaller secondary peak in the shorter wavelengths.
A study using flicker-photometric electroretinography (ERG) indicates that harbor seals possess a photopic λmax of 510 nm (Crognale et al., 1999). Furthermore,
a test for univariance also shows that harbor seals have only one cone type, a finding confirmed in a recent immunocytochemical investigation on ringed seals, harbor seals, grey seals, hooded seals, Australian fur seals, Northern fur seals, and
Southern sea lions (Peichl & Moutairou, 1998; Peichl et al., 2001).
Thus, like the cetaceans, the pinnipeds have lost their short wavelength cones,
which is surprising in a group that spends such a large proportion of its time on
land or in shallow waters. Since color vision in mammals is typically cone-based
and involves the comparison of signals from two or more cone types (Jacobs,
1993), in pinnipeds this form of color vision should not exist.
Nevertheless, several behavioral investigations show that seals make color discriminations. The first psychophysical investigation of color discrimination was
performed with a spotted seal, Phoca largha (Wartzok & McCormick, 1978). This
species has some kind of color vision because the animal discriminated between
blue and orange targets. A more detailed investigation with two species of fur
seals, Arctocephalus pusillus and A. australis, showed that the animals distinguished the colors blue and green from grey (Busch & Duecker, 1987). They
failed to discriminate red and yellow from grey. Another behavioral study using
similar methods with California sea lions (Griebel & Schmid, 1992) reported the
same results.
Color vision in marine mammals
79
Sirenia
Sirenians, or sea cows, which include manatees, dugongs and the extinct Steller's
sea cow, are aquatic herbivorous mammals which inhabit the rivers and coastal
zones of tropical seas. Little is known about their sensory apparatus or capabilities. Questions regarding their orientation, navigation, vision, taste and tactile
senses have just begun to be explored.
While anectodal comments on sirenian vision and eyes are widespread, there are
few original studies or reviews on this topic. Most of the early investigators consider sirenian vision to be very poor due to the small size of the eyes, the paucity
of retinal ganglion cells, and the apparent absence of an accommodation mechanism (Dexler & Freund, 1906; Petit & Rochon-Duvigneaud, 1929; Walls, 1942;
Rochon-Duvigneaud, 1943; Duke-Elder, 1958; Ronald et al., 1978; Piggins et al.,
1983; West et al., 1991). Hartman (1979), Gerstein (1994), and Griebel (1996)
interpret sirenian vision more positively based on their observations of visually
guided behavior in the Florida manatee. Hence, there is disagreement between an
inference based on physiological optical considerations versus ethological observations. To date, quantitative behavioral tests to resolve these questions are rare.
A detailed study on the fine structure of the retina using both light and electron
microscopy (Cohen et al., 1982) showed that the retina of the manatee
(Trichechus manatus) has both rod-like and cone-like photoreceptors. The average rod-to-cone ratio reported is 2.4:1.0. The ganglion cells have a density maximum (area centralis) in the inferior temporal quadrant of the retina (Mass at al.,
1997). The largest ganglion cells (65-90 mm) were almost exclusively concentrated in the ventral half of the eye. These large ganglion cells have also been
reported in the dolphin retina (Dawson & Perez, 1973). The terminals of cone
cells can be further subdivided into pale and moderate staining types with the
same general shape and size, and they frequently occur in pairs side by side in the
retina. These two cone types could be the S- and L-cone populations and thus present the morphological basis of cone color vision. Preliminary data (Ahnelt &
Bauer, unpublished) using antibody labeling confirm the presence of a substantial
proportion of S-cones in the manatee retina.
The only species in which the visual pigment has been extracted and measured
is Trichechus inunquis (Piggins et al., 1983). The visual pigment extraction of the
dark-adapted retina yielded a rod pigment based on vitamin A1 with a maximal
absorption at about 505 nm. Many mammals have A1-based rod pigments absorbing maximally at about 500nm; thus, the Amazonian manatee's freshwater environment has apparently not resulted in an appreciable shift of its pigment's absoption spectrum towards long wavelengths.
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Only one behavioral study has explored the color vision capabilities in this
group (Griebel & Schmid, 1996). Four manatees (Trichechus manatus) were
trained to discriminate between a colored stimulus and a shade of gray in a twofold simultaneous choice situation. The colors blue, green, red, and blue-green
were tested against shades of gray varying from low to high relative brightness.
The animals distinguished both blue and green from a series of grays but failed to
discriminate a specific hue of blue-green from certain steps of grays, suggesting
a neutral point. The colors blue, green, and red were also distinguished from each
other. The manatees were unable to discriminate between a UV-reflecting and a
UV-absorbing white target. Manatees therefore probably lack UV sensitivity and
possess color vision which is most likely dichromatic. In contrast to cetaceans and
pinnipeds, sirenians have apparently preserved the two classes of cones with two
different photopigments.
Discussion
The traditionally claimed advantage of color vision is that it promotes the perception of contrast, thus enhancing the visibility of an object in a complex surrounding. Another important advantage is color constancy. Objects in the visual
environment are typically illuminated by some combination of direct and indirect
lighting, and this can lead to significant local and temporal variations in brightness and shadowing. The variations in brightness may be substantial, whereas the
variations in color are considerably smaller. Therefore the discrimination of
objects will be more reliable if the observer can utilize color cues. The "signal significance" of colors also plays an important role and allows the observer to discern something about the nature of an object.
In the aquatic environment, the photic conditions differ in many respects from
those in air. Light intensity is lost by reflection of incident light at the surface.
Suspended particles and water molecules scatter light in all directions.
Horizontally scattered light is the reason for the even background illumination
against which objects must be recognized. Furthermore, light is scattered between
object and eye, leading to veiling and reduced contrast. Finally, the light coming
from the object is also scattered on its way to the eye. These scattering effects lead
to a strong decrease of contrast and acuity with increasing distance.
The scattering and absorption of light drastically reduce brightness with depth.
According to the type of water and the suspended and dissolved material, different wavelengths are quite variably scattered and absorbed. Surface reflection also
decreases light intensity. In the clear water of the open ocean, blue-green light
Color vision in marine mammals
81
reaches the greatest depths; in eutrophic waters, turbidity leads to a shift to the red
part of the spectrum (Jerlov, 1976, Kirk, 1994).
Thus, relative darkness, reduced contrast, and short-range visibility are characteristics of the aquatic environment. It is no surprise that dolphins have developed
the auditory sense with their echolocation system as a long-distance sensory channel and use the visual sense for short distance; in terrestrial animals it is often the
other way round. Above the surface, on the other hand, the ambient light can be
very bright due to intensive solar radiation and the reflecting water surface. We
know that dolphins and seals (and probably to some extent also the manatees) use
their eyes competently in air; their amphibious eyes must therefore adapt to a
broad range of varying light intensities. As all marine mammals feed mostly
underwater and are arhythmic, i.e. active both during the day and during the night,
they should have special adaptations for relative darkness under water.
While pinnipeds arose about 30 million years ago from carnivorous ancestors,
sirenians are believed to share a common subungulate origin with the proboscideans (Romer, 1966). Fossil evidence suggests that sirenians evolved from
primitive terrestrial herbivores early in the Tertiary. The cetaceans are also products of early land mammals and appear to have originated at about the same time
as the sirenians. The ancestry of the cetaceans is obscure, but they seem to have
derived from insectivore-creodont stock just before the divergence of the carnivore and ungulate lines (Kulu, 1972, Gingerich et. al., 1983). According to
Howell (1930), the sedentary, herbivorous life of the Sirenia has not stimulated
rapid evolutionary change, with the result that manatees and dugongs retain certain terrestrial features and are less specialized for aquatic life than cetaceans or
even the amphibious pinnipeds.
Nevertheless, the sensory abilities of marine mammals must have been readapted to the aquatic environment and to the specific needs of the three groups.
Our knowledge about the evolution of color vision in mammals remains scant.
Based on ideas drawn from natural history, Walls (1942) proposed that the receptors and photopigments necessary for color vision were lost during the nocturnal
phase of mammalian history and then re-acquired during the subsequent mammalian radiations. Contemporary examination of photopigment genes along with
the utilization of improved techniques for identifying rods and cones suggest a
different view. Accordingly, the earliest mammals had retinas containing cones as
well as rods, and two types of cone pigments: the basic mammalian color vision
was probably dichromatic (for reviews see Goldsmith, 1990; Neumeyer, 1991;
Endler, 1992; Jacobs, 1993; Ahnelt & Kolb, 2000).
The above research shows that cetaceans and pinnipeds have a very unusual
visual system among the mammals because they seem to have lost their S-cones
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completely (Crognale et al., 1998; Fasick et al., 1998; Peichl & Mountairou, 1998;
Peichl & Behrmann, 1999; Levenson et al., 2000; Peichl et al., 2001). This is quite
surprising since marine mammals, unlike terrestrial cone monochromats, have daylight activity phases. Furthermore, during dives they encounter a light environment
that is dominated by short wavelengths (Jerlov, 1976; Loew & McFarland, 1990),
so that S-cones would seem to be quite advantageous. Lythgoe & Partridge (1991)
pointed out that maximum visibility of objects under water requires two types of
photoreceptors, one matched to and the other offset from the spectral distribution
of background light against which the object has to be detected. With the loss of
the S-cones, pinnipeds and seals are limited to two receptor types (rods and Lcones) which are both sensitive in the green part of the spectrum.
Nevertheless, the loss of S-cones in two unrelated groups of marine mammals,
the cetaceans and pinnipeds, argues for convergent evolution and hence an adaptive advantage of that trait. Certainly their terrestrial ancestors had S-cones, as
indicated by the fact that recent terrestrial carnivores and artiodactyls are cone
dichromats. It has been argued (Levenson et al., 2000; Peichl et al., 2001) that the
S-opsin deletion in cetaceans and pinnipeds might be a phylogenetically old
event, stemming from an early phase in marine mammal evolution when they
most likely inhabited coastal waters. Accordingly, in the red-shifted ambient light
caused by the absorption of blue light by organic and inorganic material from land
drainage ("Gelbstoffe"), a loss of blue cones may not have constituted a significant disadvantage. Later on, when they conquered the open ocean in adaptive evolutionary radiation, this deleterious gene defect might not have been reversible;
the only remaining strategy was to shift the spectral tuning of their rods and Lcones to shorter wavelengths (Fasick & Robinson, 1998; 2000). Manatees, who
inhabit coastal waters, apparently retained cone dichromacy (Griebel & Schmid,
1996; unpublished data quoted by Ahnelt & Kolb, 2000) and are able to discriminate colors.
In pinnipeds and cetaceans, the shapes of the photopic spectral sensitivity functions suggest that rods contribute to spectral sensitivity even under ambient daylight conditions, probably by constricting the pupil to a small slit aperture, thus
maintaining a level of retinal illumination where both rods and cones can function
(Crognale et al., 1998, Griebel & Schmid, in press). This phenomenon may
explain why they are able to discriminate color even though they possess only a
single spectral cone type. The presence of two or more cone types is not a prerequisite for such discriminations. In an ERG and genetic study of the spectral
mechanisms of the nocturnal owl monkey (Aotus trivirgatus), Jacobs et al. (1993)
showed that this species is an L-cone monochromat but still capable of color discrimination, presumably through the simultaneous comparison of rod and cone
Color vision in marine mammals
83
signals. The human blue cone monochromat can also discriminate between short
and long wavelength lights (Daw & Enoch, 1973; Pokorny et al., 1979). In pinnipeds and cetaceans, color vision very likely also involves comparing rod and
cone signals. Under conditions of darkness, reduced contrast, and short visibility
in water, some crude color vision can be advantageous by enhancing contrast and
thus helping to detect objects.
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