vision colour mamalia

Aquatic Mammals 2003, 29.1, 1830

Colour vision in aquatic mammalsfacts and open questions

Ulrike Griebel1 and Leo Peichl2

1Konrad Lorenz Institute for Evolution and Cognition Research, Adolf-Lorenz-Gasse 2, A-3422 Altenberg, Austria2Max Planck Institute for Brain Research, Deutschordenstrasse 46, D-60528 Frankfurt a. M., Germany

Abstract

Aquatic mammals had to adapt to visual environ-ments that are very diVerent from those encounteredby terrestrial mammals. Herein, we review the cur-rent knowledge on the colour-vision capabilities ofaquatic mammals and discuss the puzzles thatemerge from those studies. The common pattern interrestrial mammals is dichromatic colour visionbased on two spectral types of cone photoreceptorsin the retina (commonly green and blue cones).Behavioural studies in a few pinnipeds and onedolphin species suggest a similar type of dichro-matic colour vision in marine mammals. In con-trast, recent immunocytochemical, physiological,and molecular genetic studies of the cone visualpigments in a larger sample of species show thatwhales and seals generally lack the blue cones andpresumably are green cone monochromats. Thischallenges the behavioural ndings, because conemonochromacy usually is tantamount to colourblindness. Furthermore, a loss of the blue conesseems a rather inadequate adaptation to the blue-dominated underwater light eld in the open ocean.Other aquatic and amphibiousmammals (sirenians,otters, hippopotamuses and polar bear) appear toshow the more common pattern of cone di-chromacy. The present review summarizes availabledata on the various aquatic mammalian taxa,assesses the reliability of these data, and discussesthe potential adaptive pressures involved in bluecone loss. It is suggested that blue cones were lost inan early, coastal period of cetacean and pinnipedevolution; many coastal waters preferentially ab-sorb blue light and constitute a long-wavelength-dominated environment. Residual colour vision inthese cone monochromats could be achieved inmesopic lighting conditions by exploiting the signaldiVerences between the remaining green cones andthe rods.

Key words: Colour vision, photoreceptors, retina,eye, Pinnipedia, Cetacea, Sirenia

Introduction

The ambient light conditions in the ocean diVerconsiderably from those on land and pose diVerentchallenges to the visual system. Marine mammalsprovide an excellent opportunity to study the evo-lutionary changes of the visual system in theirre-adaptation from a terrestrial to an aquatic en-vironment. The present review focuses on colourvision in marine mammals. Most terrestrial mam-mals have colour vision based on the presence oftwo spectral types of cone photoreceptors (com-monly green-sensitive cones and blue-sensitivecones), a pattern that is termed cone dichromacy.The few behavioural studies available suggest thatthe same form of dichromaticalbeit poorcolourvision occurs in marine mammals. Recently, thestory received an unexpected twist when immuno-cytochemical, physiological, and molecular geneticdata demonstrated an absence of blue-sensitivecones in the eyes of whales and seals, indicatingcone monochromacy and hence serious de citsinor even the absence ofcolour vision. This isat odds with the behavioural data. Furthermore,it seems strange that marine mammals shouldhave lost the cone type that would have beenmost sensitive to the deep blue of the open ocean.At this stage it is useful to review available data,to identify controversial and open issues, andto consider the adaptive pressures potentiallyinvolved.Marine mammals vary in the extent of their

adaptation to the aquatic environment. Cetaceansand sirenians spend all their life in water, whilepinnipeds are amphibious and divide their timebetween land and sea. Interestingly, not only theamphibious living seals, but also the whales can seewell in air. The optical and retinal structures of theeyes of marine mammals show speci c adaptationsfor vision in both media (for a recent overview,see Supin et al., 2001). The three groups of marinemammalscetaceans, pinnipeds, and sirenianshave evolved from diVerent terrestrial ancestors,belonging to the artiodactyls, carnivores, and

? 2003 EAAM

proboscideans, respectively (for recent summaries,see Gatesy & OLeary 2001; Flynn & Nedbal, 1998;Lavergne et al., 1996). We shall discuss whichproperties of the colour vision systems are inheritedfrom their respective ancestors, and which proper-ties represent convergent evolution in the en-vironmental conditions of life in the ocean. Thereview also will include references to amphibiousmammals adapted to freshwater habitats, such ashippopotamuses and otters.The term colour vision refers to the capability

of a visual system to respond diVerently to lightdiVering in wavelength only. It is based on theexistence of two or more photoreceptor types con-taining photopigments (opsins) with diVerent spec-tral sensitivity. The processing of colour-speci cinformation in the eye and brain gives rise to theperception of colour as a subjective phenomenon.The excellent colour vision of humans is based onthree spectral types of cone photoreceptorsthered, green, and blue conesand hence the arrange-ment is termed trichromatic colour vision. Mostmammals have less keen, dichromatic colour visionbased on two cone types, one maximally sensitive inthe long- or middle-wavelength range of the spec-trum (L-cone, green- to red-sensitive, depending onspecies) and one maximally sensitive in the short-wavelength range (S-cone, blue- to ultraviolet-sensitive, depending on species; reviews: Jacobs,1993; Ahnelt & Kolb, 2000).Cone monochromacy, the possession of one cone

type only and thus the absence of cone-based colourvision, is rare among mammals. It has been foundin only a few nocturnal species, while most diurnaland nocturnal terrestrial species are dichromats (forsummaries see, e.g., Jacobs, 1993; Szl et al., 1996;Peichl & Moutairou, 1998; Ahnelt & Kolb, 2000).Hence, cone dichromacy is the basic mammalianpattern and also was expected in marine mammalswhich all have daylight activity phases and appar-ently use aerial vision on a regular basis. So, it cameas a surprise that two groups of marine mammals,the pinnipeds and the cetaceans, have lost theirS-cones and become L-cone monochromats in theevolutionary process of adapting to the marineenvironment (Crognale et al., 1998; Fasick et al.,1998; Peichl & Mountairou, 1998; Peichl et al.,2001).Colour vision requires speci c neural circuits at

all levels of the visual system, starting with anappropriate set of photoreceptors and perhaps notending with colour-specic cortical neurons andareas. As Jacobs (1993) put it, ideally, [. . .] asurvey of colour vision should rely on direct evi-dence [. . .], i.e. the results of appropriately con-ducted behavioural studies. For practical reasons,behavioural research is often not possible and onehas to rely on indirect and partial evidence. Major

sources of information are physiological and mol-ecular studies of the visual pigments present in agiven species. Formally, the presence of spectrallydiVerent visual pigments is a necessary, but not asuYcient, prerequisite for colour vision. Practically,the results of cone pigment analysis commonlyagree with those of behavioural colour vision testsand hence are regarded as a robust indicator of thelevel of colour vision present. We shall come backto this issue later in the review. After a taxonomic-ally organized survey of the available data, thecrucial issues are discussed in more general termsacross orders.

Facts

CetaceaThe cetacean eye has faced several environmentalchallenges in the course of evolution. It had to bere-adapted to the mechanical, chemical, osmotical,and optical conditions of the aquatic medium.There is no doubt that dolphins are highly auditoryanimals and toothed whales in general use echo-location extensively for orientation in their naturalhabitat. Nonetheless, dolphin vision serves manyimportant biological functions, like prey detectionand capture, conspeci c and individual identi -cation, and migration and orientation. A blind-folded dolphin may have diYculty nding sh atvery close range even while echolocating.Also, theirperformance in air suggests well-developed visualfunction. Numerous learning experiments havedemonstrated that the dolphins visual system alsosupports important cognitive functions like concep-tualization and communication (Herman, 1990).The structural and functional features of cetaceaneyes and retinae have most recently been sum-marized by Supin et al. (2001). One fact quite clearfrom the available data is that cetacean eyes, despitetheir large sizes compared to those of terrestrialmammals, are not designed for high acuity. Thevisual acuity of marine dolphins is in the range of10 to 20 min of arc and hence is similar to or belowthat of many terrestrial mammals.The cetacean eye has been modi ed for high light

sensitivity. This is obvious from its complete retinaltapetalization, its large cornea, and its large pupil-lary opening that can be constricted drastically inbright light conditions above the water (Dawson,1980). The cetacean retina contains rods and cones,but is extremely rod dominated, with cone pro-portions in the range of 1%. The distributionand the frequency of the receptor types variessomewhat across species and across reports fromvarious authors (see, e.g., Ptter, 1903; Rochon-Duvigneaud, 1940; Pilleri, 1964, 1967; Pilleri &Wandeler, 1970; Perez et al., 1972; Dral, 1977;

19Colour vision in aquatic mammalsfacts and open questions

Dawson, 1980; Kastelein et al., 1990; Peichl et al.,2001).The rod visual pigments (rod opsins) of whales

use the chromophor retinal-1 as do those of othermammals, but their spectral tuning curves arebroader than those of terrestrial mammals and areshifted to shorter wavelengths (McFarland, 1971;Fasick & Robinson, 2000; Southall et al., 2002).The underwater light eld becomes successivelyblue-shifted with depth and the positions of the rodabsorption maxima (lmax) indicate an adaptationto the dominant wavelengths in the environment ofthe species, similar to the lmax ranges in manydeep-sea shes. While the rod absorption maximain terrestrial mammals are close to 500 nm, they are481 nm in Bairds beaked whale Berardius bairdi,483 nm in the sperm whale Physeter macrocephalusand Cuviers beaked whale Ziphius cavirostris,all deep diving species, 488 nm in the bottlenosedolphin Tursiops truncatus, which hunts in coastalwaters, and 496 nm in the gray whale Eschrichtiusrobustus, which bottom feeds and lives in shallowneritic waters (McFarland, 1971; Fasick &Robinson, 2000; Southall et al., 2002).Recently Phyllis Robinson and her colleagues

in Baltimore have cloned and expressed the opsingenes of the bottlenose dolphin, identifying thecDNAs for a rod opsin and a long-wavelengthsensitive (L-)cone opsin (Fasick et al., 1998; Fasick& Robinson, 1998, 2000). The resulting pigmentshad a lmax of 488 nm for the rod and of 524 nm forthe L-cone. The authors also found a gene whichcoded for a short-wavelength sensitive (S-)coneopsin, but it contained a deleterious mutation thatprevented the expression of the S-opsin protein.Deleterious S-cone opsin genes have since beenreported for further odontocete and mysticetewhales (Levenson et al., 2000; Robinson &Newman, 2002; D. L. Levenson, personal com-munication). Immunocytochemical studies usingantibodies against the S-opsin also have reported acomplete absence of the S-opsin in ten species ofodontocetes (bottlenose dolphin, common dolphin,white-beaked dolphin, Rissos dolphin, striped dol-phin, long- and short- nned pilot whale, harbourporpoise, Dalls porpoise, and northern bottlenosewhale), while con rming the presence of L-cones inall these species (Peichl et al., 2001; 2002). Takentogether, these data suggest that toothed and baleenwhales are L-cone monochromats and hence shouldlack the dichromatic form of colour vision typicalfor most terrestrial mammals.To date, electrophysiological studies on cetacean

spectral sensitivity and colour vision are non-existent and behavioural investigations are ex-tremely rare, because animals are rarely availablefor such experiments and behavioural studies arevery time-consuming.But, as noted in the introduc-

tion, the only way to demonstrate that an animalactually uses colour information is to perform be-havioural experiments. The rst behavioural studyon colour vision in cetaceans was done by Madsenwith a bottlenose dolphin (Madsen, 1976; Madsen& Herman, 1980). The animal had to discriminate acoloured light from a white light and also twocoloured lights from each other (the stimuli werevaried in intensity), rst in a go/no-go discrimi-nation task, and then in a successive two-choicediscrimination task with one stimulus eld and tworesponse paddles. In both protocols, the colourstimuli were used as cues in a spatial reversalproblem. Under these conditions the experimentaldolphin did not demonstrate colour discrimination.Madsen (1976) calculated the spectral sensitivity

curve on the basis of a brightness match between ared, a green, and a blue monochromatic light. Thedolphins spectral sensitivity function peaked at500 nm under photopic conditions and shifted to496 nm under scotopic conditions. This result indi-cated a rod and a green cone mechanism. Thescotopic shift is not very large, suggesting thatthe conditions might have been only mesopic forthe dolphin, since the experiment was conductedunder the night sky. The scotopic peak at 496 nmwas 10 nm red-shifted from the lmax of the ex-tracted rod pigment of Tursiops (486488 nm;McFarland, 1971; Fasick et al., 1998). Similarly, thephotopic peak at 500 nm was 24 nm blue-shiftedfrom the lmax of the L-cone pigment (524 nm;Fasick et al., 1998). Behavioural or ERG sensitivitycurves often show a shift with respect to the absorp-tion maxima of the corresponding isolated pigmentsbecause of the spectral properties of the eye media,or incomplete dark or light adaptation (seeMethodological Aspects below).A recent behavioural study re-examined dolphin

spectral sensitivity (Griebel & Schmid, 2002). In alight-adapted bottlenose dolphin, spectral sensitiv-ity was measured in air in a spectral range from397 nm to 636 nm in a simultaneous two-choicediscrimination test by determining incrementthresholds. The resulting spectral sensitivity curvewas very broad, suggesting the contribution ofmore than one pigment and showed a sensitivitymaximum in the blue-green part of the spectrumat about 490 nm. Since dolphins have lost theirS-cones, the second pigment contributing to thespectral sensitivity function is probably the rodpigment. Interestingly, the curve tilted upwardagain in the near ultraviolet, suggesting a secondmaximum in the near UV. Two wavelength dis-crimination tasks, where brightness was adjusted tothe subjective spectral sensitivity of the dolphin,showed that the dolphin could discriminate between397 nm and 487 nm, but not between 457 nm and544 nm. This result suggested that a mechanism for

20 U. Griebel and L. Peichl

colour discrimination is present even in the absenceof S-cones.For baleen whales, there exist no behavioural,

physiological, or immunocytochemical data on col-our vision capabilities, spectral sensitivity or coneopsins. The only available information is that thespecies studied to date have deleterious S-opsingenes and hence no functional S-cones (Levensonet al., 2000). This suggests L-cone monochromacyalso occurs in baleen whales.

PinnipediaUnlike the cetaceans and manatees, pinnipeds areamphibious and spend a substantial portion of theirtime on land for resting, giving birth, mating, andmoulting. Like cetaceans, many pinnipeds also ex-perience low light levels when diving or foraging atnight. They did not evolve echolocation, but theypossess very sensitive vibrissae which they use forturbulence tracking (Dehnhardt et al., 1998; 2001).As indicated by their big eyes, vision plays asigni cant role in pinnipeds for various biologicalfunctions like hunting, orientation, and communi-cation. As members of the carnivore order, pinni-peds have rather frontally positioned eyes and anextended binocular eld-of-view that suggests gooddepth perception. The structural and functionalfeatures of pinniped eyes and retinae have mostrecently been summarized by Supin et al. (2001).Visual acuities of seals and sea lions are in the rangeof a few minutes of arc. This reasonably goodacuity is similar to that of terrestrial carnivores, e.g.dogs and cats.In adaptation to low-light conditions, the eyes of

pinnipeds have well-developed tapeta behind mostof the retinal area (Braekevelt, 1986). Their retinaeare densely populated with highly light-sensitiverods, but also contain sparse populations of cones,constituting about 1% of the photoreceptors(Landau & Dawson, 1970; Jamieson & Fisher,1971; Nagy & Ronald, 1975; Mass, 1992; Peichl &Moutairou, 1998; Peichl et. al., 2001, 2002). Behav-ioural evidence also suggested a duplex retina fea-turing a Purkinje shift, a break in the dark adaptioncurve (Lavigne & Ronald, 1972; Levenson &Schusterman, 1998) and a break in the critical icker-frequency curve (Bernholz & Matthews,1975).The spectral absorption curves of pinniped rod

visual pigments are shifted to shorter wavelengthsthan those of terrestrial mammals, with a lmax atabout 496 nm in the shallow diving California sealion Zalophus californianus and harbour seal Phocavitulina, and a lmax of 483 nm in the deep divingnorthern elephant seal Mirounga angustirostris(Lythgoe & Dartnall, 1970; Lavigne & Ronald,1975; Lavigne et al., 1977; Fasick & Robinson,2000; Southall et al., 2002). Furthermore, the rod

system in the last-mentioned species seems to beable to adapt extremely fast, attaining its thresholdsensitivity within 6 min (Levenson & Schusterman,1999). So, pinniped rod pigments, like those ofcetaceans, appear to be adapted to diving depth.The behaviourally measured photopic spectral

sensitivity of the harp seal showed a main maxi-mum at 550 nm and a secondary peak near 480 nm(Lavigne & Ronald, 1972). A behavioural studyof photopic spectral sensitivity in the harbour sealand southern sea lion (Otaria byronia) yieldedsimilar results (peak sensitivities around 500 nmand around 540 nm, respectively: Griebel, Knig &Schmid, submitted). In both studies, the main peakindicating an L-cone was very broad, suggesting thecontribution of a second pigment type (probablythe rod pigment). The secondary, short-wavepeak in all these behavioural curves suggested thepresence of a second, short-wave sensitive (blue)cone.The sensitivity picture has been corroborated by

behavioural studies on colour discrimination. The rst psychophysicalinvestigationof colour discrimi-nation was performed with a spotted seal, Phocalargha (Wartzok & McCormick, 1978). The resultssuggested that this species has some kind of colourvision since the animal discriminated between blueand orange targets. A more detailed investigationwith two species of fur seals, Arctocephalus pusillusand A. australis, showed that the animals were ableto distinguish blue and green from grey, but failedto discriminate red and yellow from grey (Busch &Duecker, 1987). Another behavioural study usingsimilar methods with California sea lions reportedthe same results (Griebel & Schmid, 1992).In contrast, a study using icker-photometric

electroretinography (ERG) indicated that harbourseals possess a photopic lmaxof 510 nm and showedby a test for univariance that this species has onlyone cone type, the L-cone (Crognale et al., 1998).Immunocytochemical studies with antibodiesagainst the opsins of L- and S-cones in eight speciesof phocids and otariids also demonstrated a com-plete absence of S-cones in all these species, whileL-cones were present at the expected low densities[species studied: ringed seal (Phoca hispida), har-bour seal, grey seal (Halichoerus grypus), hoodedseal (Cystophora cristata), bearded seal (Erignathusbarbatus), Australian fur seal, northern fur seal, andsouthern sea lion; Peichl & Moutairou, 1998; Peichlet. al., 2001; 2002]. Interestingly, the genetic basisfor the S-opsin loss appears to diVer among sealspecies. The harp seal (Phoca groenlandicus)likethe cetaceans referred to abovehas a defectiveS-opsin gene, whereas the harbour seal has an intactS-opsin gene, but no retinal S-opsin mRNA,suggesting deleterious mutations at the promoter orsplice site level (Robinson & Newman, 2002).


The conclusion from the physiological, cellular,and genetic evidence is that, like the cetaceans, thepinnipeds have lost their S-cones and only retainedthe L-cones. Since colour vision in mammals istypically cone-based and involves the comparisonof signals from two or more cone types, in pinni-peds this form of colour vision should not exist.That is surprising in a group spending a largeproportion of time on land or in shallow waters,where the light is spectrally broad and would allowcolour vision.

SireniaSirenians, which include manatees, dugongs and theextinct Stellers sea cow, are aquatic herbivorousmammals which inhabit the rivers and coastal zonesof the tropical seas. They have nocturnal anddiurnal activity phases. Little is known about thesensory apparatus or capabilities of sirenians. Ques-tions regarding their orientation, navigation, vision,taste, and tactile senses have just begun to beexplored. The available data have been summarizedrecently by Supin et al. (2001). While most of theearly investigators considered sirenian vision to bevery poor, a more favourable view now hasemerged from observations of visually guided be-haviour in the Florida manatee Trichechus manatus(Hartman, 1979; Gerstein, 1994; Griebel & Schmid,1996). Although there are earlier contradictoryreports about the presence of a tapetum in thesirenians, there seems to be no tapetum lucidum inthe manatee eye (Piggins et al., 1983; P. Ahnelt,personal communication).A light and electron microscopic study of the

Trichechus manatus retina revealed both rod-likeand cone-like photoreceptors (Cohen et al., 1982).The average cone-to-rod ratio reported was 1:2.4,indicating a much greater importance of cone-basedvision than in cetaceans and pinnipeds. Actually,the cone proportion of some 30% appears improb-ably high for an arhythmic mammal, because evenmost diurnal species have only 515% cones. Fur-ther investigation is needed in this case. Preliminaryimmunocytochemical data indicate the presence ofboth L-cones and S-cones in the manatee retina(Ahnelt & Bauer, personal communication). Re-cently, a genetic analysis of the manatee has estab-lished the presence of intact S-opsin and L-opsingenes, which are expressed in the retina (Robinson& Newman, 2002). All this argues for the presenceof cone-based dichromatic colour vision.The rod visual pigment has been analyzed in

the Amazon manatee Trichechus inunquis (Pigginset al., 1983). The extracted rod visual pigment isbased on retinal-1 and has a lmax of about 505 nm.Given that many terrestrial mammals have a rodpigment lmax close to 500 nm, the manatees

freshwater environment has probably resulted in aslight red-shift of its rod pigment.At present, there is only one behavioural study

exploring the capabilities for colour vision in thisgroup (Griebel & Schmid, 1996). Four Trichechusmanatus individuals were trained to discriminatebetween a coloured stimulus and a shade of grey ina two-fold simultaneous choice situation. The col-ours blue, green, red, and blue-green were testedagainst shades of grey varying from low to highrelative brightness. The animals distinguished bothblue and green from a series of greys, but failed todiscriminate a speci c hue of blue-green from cer-tain steps of greys, suggesting a neutral point typi-cal for cone dichromats. The colours blue, green,and red also could be distinguished from eachother. These results suggest conventional dichro-matic colour vision. The manatees could not dis-criminate between a UV-re ecting white target andan UV-absorbing white target. In summary, allavailable evidence indicates that, in contrast tocetaceans and pinnipeds, manatees have preservedthe two spectral classes of cones. We are not awareof any data on the cone types and colour vision ofdugongs, the other extant sirenian clade.

Other amphibious mammalsWhen searching for the environmental pressuresthat led to a loss of the blue cones in cetaceans andpinnipeds, but not in sirenians, it is instructive tolook at other mammals that have partly adapted tofreshwater or seawater, i.e. amphibious mammalianspecies. Most prominent among them are the artio-dactyl hippopotamuses, and two carnivore groups,the otters and polar bears. Because the pinnipedsare carnivores and the cetaceans are closely relatedto the artiodactyls, one can assume common ances-tral photoreceptor equipments and hence, con -dently attribute observed diVerences to diVerentadaptive pressures.

OttersThe amphibious otters (mustelid carni-vores) live in rivers, lakes, or close to the sea shore.Unlike the river otters (Lutra spp.), the sea otter(Enhydra lutris) rarely ever leaves the water andstays most of its life close to the sea shore, seekingprotection in kelp beds. River otters are activeduring both day and night and feed mostly on sh.Behavioural observations (Erlinge, 1968) and ex-periments (Green, 1977) have shown that the riverotter hunts predominantly by vision. Green (1977)showed that the otter takes four times longer to ndprey in turbid water than in clear water. Withoutvibrissae the time necessary to nd the prey staysthe same in clear water, but takes 20 times longer inturbid water.River otters (Lutra lutra) possess an extensive

tapetum lucidum cellulare and the retina contains


rods and cones (Pilleri, 1967). There are S-cones aswell as L-cones in low densities, thus showing thetypical mammalian dichromatic pattern (Peichlet al., 2001). Behavioural experiments with L. lutra,carried-out in shallow water, have shown that itcan discriminate the colours blue and green fromvarious shades of grey (Kasprzyk, 1990). TheSoutheast Asian river otter (Amblonyx cineriacineria) was able to discriminate red and greenfrom greys (Balliet, 1970). In the sea otter, Mass& Supin (2000) have analyzed the retinal ganglioncell distribution and derived a retinal resolution(visual acuity) of about 7 min of arc in water. Weare not aware of any colour vision studies in seaotters.

Polar bearThe preferred habitat of polar bears(Thalarctos maritimus, an ursid carnivore) is thepack ice, so much so that it has resulted in a whitefur as an adaptive coloration. The polar bearspreferred food is ringed seal, which it commonlyhunts on ice or at the waters edge. Polar bears aregood swimmers and in water also feed on sea birdsand sh. Hence, they can be considered well-adapted to marine life. Polar bears are active undervarious illuminations from bright sunshine on snowto mid-winter darkness, but there is little infor-mation on their visual abilities and on the extent towhich they depend on sight (for references, seeRonald & Lee, 1981). The visual environment of thepack ice zone is dominated by shades of white andgrey and oVers hardly any opportunity for colourvision.Nevertheless, the only available study on polar

bear spectral sensitivity, which is a behavioural one,reports a bimodal photopic curve with peaks at525 nm and 450 nm, suggesting the presence ofL-cones and S-cones (Ronald & Lee, 1981). Thescotopic sensitivity peaks at 525 nm, suggesting ared-shifted rod pigment. So, we assume that thepolar bear is a normal cone dichromat, while fur-ther studies are necessary to rmly establish theexistence and extent of its colour vision capabilities.

HippopotamusVery little is known about thevisual system of the hippopotamus (Hippopotamusamphibius), an African amphibious freshwatermammal that spends most of its time in rivers andlakes and only leaves the water during the nightfor grazing. Luck (1965) described cones in thehippopotamus retina. An immunocytochemical as-sessment of the cone opsins in the pygmy hippo-potamus (Choreopsis liberiensis) has demonstratedthe presence of S-cones and L-cones (Peichl et al.,2001). This suggests normal dichromatic colourvision, but to date no behavioural experiments havebeen done.

Discussion

Two puzzlesRegarding whales and seals, two obvious puzzlesemerge from the above survey. First, there is theapparent contradiction between the photoreceptordata indicating cone monochromacy, and the be-havioural data indicating some capacity for colourvision. Here, one has to critically examine thereliability of various data and to consider whethercolour vision is at all possible with just one conetype. The second puzzle is the loss of the blue-sensitive cone type in an environment that is domi-nated by blue light, i.e. the sacri ce of a seemingly tting photoreceptor. What are the actual viewingconditions in diVerent waters, what is potentiallygained by the blue cone loss, and what are theevolutionary paths involved? These are the issuesfor the remaining sections of this review.

Methodological aspects

Immunocytochemistry, genetics, physiologyTheevidence for the absence of S-cone opsin in whalesand seals is convincing. The most convenientmethod to identify cone opsins across a largenumber of species has been immunocytochemicallabelling of the L- and S-cones with opsin-speci cantibodies. As discussed in Peichl et al. (2001), theantibodies used in these studies have proven toreliably label the respective opsins in a wide rangeof species across mammalian orders, speci cally interrestrial species that are closely related to thewhales and pinnipeds. One might argue that theS-opsins of marine mammals are molecularlymodi ed to an extent that prevents recognition bythe antibodies. However, given the reliability ofthe labelling across distant mammalian taxa, thisseems unlikely. For the ringed seal, it has beenshown directly that all cones contain the L-opsin,i.e. there are no cones with an unidenti ed opsin(Peichl & Moutairou, 1998). Another concern ispoor tissue preservation, since specimens fromstranded animals often have been xed relativelylate post mortem and stored in a xative for ex-tended periods. So, photoreceptor outer segmentscould have been damaged or opsins decomposed.However, the presence of L-opsin immunoreactivityin the same tissue and the successful labellingof S-opsin in terrestrial mammalian tissue thathad been similarly treated, argues against tissuepreservation being a critical factor.Support for the immunocytochemicaldata comes

from genetic studies performed in some species(Fasick et al., 1998; Fasick & Robinson, 1998;Levenson et al., 2000; Robinson & Newman, 2002).They showed that S-opsin genes are present in allthe seals and whales studied, but that these genes


contain deleterious mutations preventing expres-sion of the opsin protein. This provides a proximalexplanation for the lack of S-cones. It also indi-cates that the ancestors of whales and seals oncepossessed S-cones.One property of the available opsin antibodies is

that they label any member of the S-opsin orL-opsin family, irrespective of the exact spectralsensitivity of the visual pigment. Generally, this isadvantageousbecause the labelling is not subject tospecies-specic spectral shifts. The S-opsin anti-bodies label the blue-sensitive S-cones of carnivoresand ungulates, as well as the UV-sensitive S-conespresent in some rodents. The L-opsin antiserumlabels green-sensitive, as well as red-sensitiveL-cones. But, there is a shortcoming. If whales orseals had more than one spectral opsin type belong-ing to the L-opsin family, the L-opsin antiserumwould label them indiscriminately. So, one mightargue that whales and seals could have two L-conetypes and thus, dichromatic colour vision despitethe absence of S-cones. However, this possibility isruled-out by the genetic data showing only oneL-opsin gene product. Furthermore, an ERG studyin the harbor seal demonstrated that its photopicspectral sensitivity curve is best tted by a single(green) cone opsin absoption curve (Crognale et al.,1998). It also should be noted that L-opsin poly-morphism has not been reported in any mammaloutside primates.Taken together, the cellular data provide sound

evidence for an S-cone loss in a substantial numberof whales and seals. Even though the sample ofspecies is small (e.g. baleen whales are distinctlyunder-represented), it is broad enough to put for-ward the working hypothesis that cetaceans andpinnipeds have generally lost their S-cones and areL-cone monochromats.

BehaviourTwo types of behavioural experimentson colour vision have been performed.One involvesa colour discrimination task where the animal istrained to discriminate various coloured stimulifrom grey stimuli or other colour stimuli in aforced-choice situation. DiVerent shades of greyfrom low to high relative brightness, and/or colourstimuli varying in brightness, are tested against eachcolour to rule-out the possibility that the animaluses brightness cues to succeed in the task. Thesecond is a measurement of the spectral sensitivityfunction, where the animal is trained to respond tofaint monochromatic light stimuli across the visiblespectrum. The detection threshold for stimulus in-tensity at each wavelength is determined to obtainthe spectral sensitivity curve. Both methods can beperformed at photopic and scotopic ambient lightlevels to obtain cone- and rod-based performance,respectively. The rst method directly tests the

ability to discriminate colours. The second onlymeasures the sensitivity to various wavelengths,giving information on the spectral characteristics ofthe photoreceptors and visual pigments involved,but this method cannot determine whether theanimal uses these signals for colour vision.Behavioural colour vision experiments are notori-

ously diYcult and conditions are less stringentlycontrollable than in cellular studies. First, the ani-mal has to cooperate, i.e. it has to respond to astimulus it perceives. The variability across individ-uals reported in many of the marine mammalstudies shows that this problem is not negligible.However, while a negative result could merely indi-cate that the animal has not understood or at-tended to the task, a positive result is more reliable.Second, one has to rule-out the possibility that theanimal uses brightness cues instead of colour cuesto discriminate stimuli. The perception of relativebrightness varies across species, so as a startingpoint one has to assess the appropriate stimulusparameters for each species. Our knowledge ofthese parameters has continuously increased, suchthat recent studies are commonly better controlledand hence more reliable than the older studies.Third, photopic and scotopic conditions have to bede ned for each species to obtain pure cone- orrod-driven responses. Mesopic conditions, inter-mediate between scotopic and photopic light levels,are those where both rods and cones are in theirworking range. Depending on pupillary mechan-isms, the optical properties of the eye media, thepresence of a re ecting tapetum, etc., an illumi-nation level that is scotopic for a human observercould be mesopic for another species, and vice versaa human photopic level could be mesopic for someother species. As we shall see below, an interactionbetween rods and cones can provide some colourvision even in cone monochromats. Many behav-ioural studies on marine mammal colour visionhave assumed photopic or scotopic conditionswith-out being able to prove that they were operativeduring the tests.A further diYculty is found in correlating the

maxima of behavioural spectral sensitivity curveswith the spectral absorption maxima of isolatedvisual pigments. The spectral transmission proper-ties of the eye media, the interaction of rods andcones at mesopic light levels, the processing charac-teristics of postsynaptic retinal neurons, and furtherfactors often result in shifts of behaviourally deter-mined sensitivity maxima with respect to those ofthe underlying visual pigments. It is sometimesplainly impossible to reconcile the two sets of data.The harp seal could serve as an example in case. Itsbehavioural photopic and scotopic sensitivity func-tions were measured by Lavigne & Ronald (1972).The photopic curve has two maxima near 550 nm


(yellow-green) and 480 nm (blue). Does this indi-cate two cone types, one green-sensitive and oneblue-sensitive? Recent evidence showed that theharp seal has no blue cones (Robinson & Newman,2002; Peichl, unpublished observations). The be-havioural scotopic curve has a maximum near520 nm, with a secondary bulge at 450 nm (Lavigne& Ronald, 1972). But, the rod opsin of the harp sealhas a lmax of 497 nm (Lavigne & Ronald, 1975).Could the testing conditions have actually beenmesopic, such that both the photopic and thescotopic curve contain cone and rod contri-butions? In the photopic curve, a 497 nm rod wouldnot explain the 480 nm secondary maximum. Inthe scotopic curve, an L-cone contribution mightexplain the long-wave shift from 497 nm to 520 nm,but there is no S-cone to explain the 450 nm bulge.Hence, the blue sensitivity in the behavioural curvesremains a puzzle.

Can cone monochromats see colour?The ability to discriminate colours requires theexistence of two or more spectral photoreceptortypes. As a rule these are the cones, because forphysical and biochemical reasons colour vision re-quires a certain amount of light intensity, i.e., asubstantial photon ux onto the photoreceptors, toincrease the signal-to-noise ratio. Colour vision ismost acute in photopic conditions, when input intothe visual system comes exclusively via the cones.But, colour vision (somewhat reduced) also is poss-ible in mesopic conditions, when the cone signalsare less strong. This is the light level where theworking ranges of cones and rods overlap, andwhere rod signals, which are spectrally diVerentfrom those of the cone(s), might be included inneural computations to extract colour information.In fact, rod contributions to colour vision

have been demonstrated. The owl monkey (Aotustrivirgatus), one of the few terrestrial L-conemonochromats, has residual colour vision undermesopic conditions and this has been attributedto the interaction of the rods and the persistingL-cones (Jacobs et al., 1993). Human S-conemonochromatspeople with a rare genetic disorderwho have no red and green cones, just blue conesand rodscan distinguish wavelengths in the rangeof 440 to 500 nm with near-normal precision, pro-vided the ambient illumination is mesopic (Reitneret al., 1991). Beyond 500 nm, wavelength discrimi-nation deteriorates rapidly, and in photopic con-ditions wavelength discrimination breaks downcompletely. This indicates that the discrimination ismade by using S-cone and rod signals, which is notpossible at photopic light levels. The human rodhas a lmax of about 500 nm and the S-cone ofabout 420 nm, explaining the good wavelength

discrimination in the 440 to 500 nm range and itsfailure at longer wavelengths.Hence, in principle, colour vision is possible for

cone monochromats. But, it is restricted to mesopiclighting conditions where the rods can contributeand it appears to be spectrally limited by theabsorption curves of the rod opsin and the availablecone opsin. For marine mammals with a rod lmaxbetween 481 and 500 nm and an L-cone lmaxbetween 510 and 525 nm (depending on species,see above), one would predict colour discriminationin the rather narrow wavelength range of about480 to 520 nm (blue-green part of the spectrum)and a failure to discriminate shorter or longerwavelengths. This prediction is compatible withthe behavioural ndings that fur seals and theCalifornia sea lion can discriminate blue and greenfrom grey, but not red and yellow from grey (Busch& Duecker, 1987; Griebel & Schmid, 1992).We also reason that the behavioural studies re-

porting colour vision in seals and whales must infact have been conducted at mesopic light levels,even when photopic conditions were assumed bythe investigators. Mesopic, rod-cone colour dis-crimination oVers the most parsimonious expla-nation to reconcile the behavioural results with thedemonstration of L-cone monochromacy, as hasbeen suggested by Crognale et al. (1998).

Vision in the marine environmentIn trying to understand why cetaceans and pinni-peds, but not other aquatic and amphibious mam-mals, have lost their short-wave sensitive cones andthus jeopardized colour vision, we look to thespeci c conditions of vision in aquatic environ-ments. The traditionally claimed advantage ofcolour vision is that it promotes the perception ofcontrast, thus enhancing the visibility of an objectin a complex surrounding. Another advantage iscolour constancy. Objects in the visual environmentare typically illuminated by some combination ofdirect and indirect lighting and this can lead tosigni cant local and temporal variations in bright-ness and shadowing. Variations in brightness maybe substantial, whereas the variations in colour areconsiderably smaller. Therefore, the discriminationof objects will be more reliable if the observer usescolour cues. Also, the signal signi cance of coloursplays an important role and allows the observer todiscern something about the nature of an object.In the aquatic environment, the photic conditions

diVer in many respects from those in air. One aspectis image quality. Suspended particles and watermolecules scatter light in all directions. These scat-tering eVects, much more pronounced in water thanin air, lead to a strong decrease of contrast andacuity with increasing distance (Jagger & Muntz,1993). Another aspect is the intensity and spectral


compositionof the available light. Some light inten-sity is lost by re ection of incident light at the watersurface, and the scattering and absorptionof light inthe water drastically reduce brightness with depth.Depending to the type of water and the suspendedand dissolved material, diVerent wavelengths arevery diVerently scattered and absorbed. In the clearwater of the open ocean, blue light (450480 nm)penetrates deepest; in eutrophic waters, turbidityleads to a shift towards the red part (around600 nm) of the spectrum (Jerlov, 1976; Kirk, 1994).Thus, relative darkness, a narrow spectrum, re-

duced contrast, and short-range visibility are char-acteristics of the deeper aquatic environment. Aswhales and seals make most of their living underwater and are also arhythmic, i.e. active duringthe day as well as during the night, they shouldhave special adaptations for relative darknessunder water. Examples for such adaptations arestrong rod dominance and the presence of re ectingtapeta in all whales and pinnipeds and unusuallyrapid dark adaptation in deep-diving pinnipeds(Levenson & Schusterman, 1999). One can con-clude that the dominant pressure on the visualsystems of whales and seals was for optimizingscotopic, rod-mediated vision.Nevertheless,whales and pinnipeds have retained

a small population of cones to cope with higherlight intensities, as have all nocturnal terrestrialmammals, which are similarly adapted to scotopicvision. The stunning diVerence is that most noctur-nal terrestrial mammals have L-cones and S-conesand hence, the potential for dichromatic colourvision, whereas all whales and seals studied to dateare L-cone monochromats. If this diVerence is dueto the aquatic environment, it appears paradoxical.Even if colour vision is not an issue in a relativelymonochrome blue underwater environment, theS-cones would be better suited than the L-cones todetect intensity and contrast cues. Matched pig-ments are postulated by the sensitivity hypothesisof F. W. Munz, implying that for optimal sensitiv-ity visual pigments should be tuned to the availablewavelengths (review: Lythgoe & Partridge, 1991).This is emphasized by the fact that the spectralsensitivities of the rods and L-cones of many marinemammals are somewhat blue-shifted from those ofterrestrial mammals, suggesting an adaptive movetowards the available wavelengths. The broad spec-tral absorption curves of the L-opsins actuallyextend into the blue part of the spectrum, albeitwith reduced sensitivity. So why have the S-conesand not the L-cones been lost?

Some hypotheses

OVset pigmentsOne explanation for a spectralmismatch between visual pigments and the under-

water light eld was proposed by Lythgoe (review:Lythgoe & Partridge, 1991). This contrast hypoth-esis implies that oVset pigments with longer-wavelength sensitivity than that of the blue ambientlight would improve the detection of contrast be-tween an object and the backgroundprovidedthat the objects re ection is spectrally broader thanthe background light. However, this condition onlyholds for re ective objects (e.g., sh) viewed hori-zontally at short ranges in shallow water, where thedownwelling light re ected by the object has ashorter path length in water to the observers eyeand hence is spectrally broader than the back-ground light and the veiling light that travels alonger distance through the waters blue spectral lter. In all other casesobjects darker than thebackground, and both bright and dark objects indeep water or at longer distances or seen frombelowthe advantageof oVset pigments disappearsand matched pigments are more eYcient. Lythgoe& Partridge (1991) concluded that retinae contain-ing matched as well as oVset pigments would beoptimally equipped for all potential underwaterviewing conditions. Clearly, this is not the case inwhales and pinnipeds.

Chromatic aberrationAnother line of argumentconsiders optical reasons for L-cone mono-chromacy. Highly light-sensitive eyes require anaperture (pupil) that is large in relation to the focallength of the eye. This leads to a very short depth offocus, often much shorter than the diVerences infocal length for the diVerent wavelengths (termedlongitudinal-chromatic aberration), and only anarrow band of wavelengths can be simultaneouslyin focus on the retina. A number of shes andterrestrial vertebrates have solved this problemof chromatic defocus with multifocal lenses. Eachfocal length of the lens creates a sharp image forone of the spectral cone types (Krger et al., 1999;Krger, 2000). However, such a mechanism sacri- ces sensitivity and contrast for improved colourdetection. Maximal light gathering can only beachieved with monofocal lenses. With these, allphotoreceptors should have similar spectral sensi-tivities, because other wavelengths are out of focus.As the lmax of the rods, which are the crucialphotoreceptor type in highly sensitive eyes, is closerto the lmax of the L-cones than to that of theS-cones, the latter could have been lost becausethere was no useful image in their spectral sensitiv-ity range. The properties of marine mammal lenseshave yet to be determined to test this hypothesis.Also, it is unclear why nocturnal terrestrial mam-mals, which are faced with the same demands onlight sensitivity, have not taken the same path, butinstead have retained both cone types.


Tapetum lucidumThe tapetum lucidum, a re ec-tive layer behind the retina, greatly increases lightcapture by the retina but it also acts as a spectral lter, evidenced by its colour when observed inwhite light. Both the pinnipeds and the whales havetapeta like their terrestrial relatives, the carnivoresand artiodactyls. Could the spectral narrowing ofthe available light by the tapetum have led to theloss of the S-cones? The cats tapetum, which isgreen or yellow (depending on the individual), has ahigh spectral re ectance in the 500600 nm rangeand a steeper decrease towards the blue than thered end of the spectrum. Nevertheless, the spectralsensitivity of the cats retina, measured by ERG,shows no diVerence between tapetal and non-tapetal regions (cat data reviewed in Muntz, 1972);and, the cat has L- and S-cones. Hence, the tapetumdoes not exert a signi cant in uence on spectralsensitivity or cone types. The tapeta of artiodactyls(also possessing L- and S-cones) have individuallyvarying green, yellow, and sometimes blue regions.In odontocetes, the tapetal colours of xed eyes

were reported to diVer among species, individualsand fundus regions, covering the range from yellowto green to blue to whiteish (Ptter, 1903; Dawson,1980). Some of this range can be attributed to xation-induced changes. The in vivo colouration ofthe tapetum has been assessed in Tursiops truncatusand Grampus griseus (Dawson et al., 1987). Here,Tursiops has a green-yellow tapetum with littleinter-individual variation; the tapetum of Grampushas a more blue-shifted appearance. The study alsogives spectral measurements, indicating high re ect-ance in the 500700 nm range and low re ectancebelow 500 nm in Tursiops, and high re ectance for450700 nm light in Grampus. Qualitatively, this isnot too diVerent from the situation in the cat.Most ( xed) pinniped tapeta seem to be dull

blue-grey, while metallic yellow in the genus Phoca(Ptter, 1903). Hence, depending on species, thetapeta of whales and seals are similar to or blue-shifted from those of terrestrial mammals, perhapsindicating some adaptation to the underwater en-vironment. Extrapolating from the cat ndingsabove, one can assume that such tapeta would notput the blue cones at a disadvantage and thuscannot explain the S-cone loss.

S-Cone loss an ancient adaptation?The above hypotheses are worth following up, butat present they do not give satisfactory explanationsfor the S-cone loss. One reason is that the lossoccurs in shallow and deep divers, in coastal and inopen sea dwellers, in the purely aquatic whales andthe amphibious pinnipeds, i.e., in species that areexposed to rather diVerent photic environments.Should that not have imposed diVerent adaptivepressures, favouring an S-cone loss in some species,

but not in others? To overcome this dilemma, wehave hypothesized that the S-cone loss may not berelated to adaptive pressures in the present habitats,but may have occurred rather early in the evolutionof whales and pinnipeds in adaptation to a diVer-ent, more uniform photic environment (Peichl et al.,2001).The basic mammalian pattern is cone dich-

romacy. In particular, modern terrestrial artio-dactyls and carnivores are conventional dichromatswith L-cones and S-cones (comparative overviews:Jacobs, 1993; Szl et al., 1996; Ahnelt & Kolb,2000). Thus, it can be assumed that the terrestrialancestors of whales and pinnipeds had S-cones.This is supported by the persisting presence of theS-opsin genes, albeit defective. The parallel loss ofthe S-cones in the marine members of two distinctorders, but not in their terrestrial close relatives,argues for convergent evolution and an adaptivepressure exerted by the marine habitat. The absenceof S-cones in all pinnipeds and all cetaceans studiedto date suggests an early occurrence of the geneticchange, which then spread throughout their respec-tive radiations. So, the most likely time was shortlyafter the return of ancestral whales and seals to thesea. During this initial, partly amphibious phase,they are thought to have inhabited coastal waters(Gingerich et al., 1983).In many coastal marine waters, the underwater

light spectrum is red-shifted due to blue lightabsorption by organic and inorganic materialfrom land drainage and biological debris (gilvins,GelbstoVe); even at relatively shallow depthsand photopic light levels, there is little blue lightremaining (Dartnall, 1975; Jerlov, 1976; Loew &McFarland, 1990). In such conditions, a loss of thejobless blue cones may not have constituted asigni cant disadvantage and could even have beenan economical adaptation, simplifying retinal andcortical visual information processing. Some de-scendant species have stayed in coastal waters andfor these the S-opsin loss remains useful or at leastneutral. Other descendant species have later con-quered the open ocean in adaptive evolutionaryradiation. They might now have pro ted from afunctional S-opsin, but they could not reverse thedeleterious gene defect. All they could apparentlydo was shift the spectral tuning of their remainingphotoreceptors to shorter wavelengths.Assuming a loss of the S-cones shortly after

the emergence of cetaceans and pinnipeds, respect-ively, we originally thought that the underlyinggenetic change should be rather similar (homolog)within each order while diVering between theorders (Peichl et al., 2001). However, recent prelimi-nary evidence suggests diVerent genetic loci ofthe defect in two phocids (Robinson & Newman,2002) and some whales (D. H. Levenson, personal


communication). One might conclude that withineach order the S-cone loss occurred independentlyseveral times. Another, more parsimonious inter-pretation is that within each order a common, as yetunidenti ed genetic change, e.g., in the promoter ofthe S-opsin gene, exists in all species, thwarting theexpression of an S-opsin protein and hence allowingsecondary, species-speci c mutations to accumulatein the gene itself (L. Newman & P. Robinson,personal communication). Further data are neces-sary to test these hypotheses and to decide betweenthe one event and the multiple independentevents scenarios. It also could be possible to iden-tify the time point(s) of S-cone loss and to check forcoincidence with the early coastal period. Whilemultiple, independent losses of S-cones would em-phasize the power of the adaptive pressures in-volved, they also leave open the possibility thatsome cetacean or pinniped may yet be found tohave kept its S-cones.The manatees, which live in a coastal habitat,

seem to have retained cone dichromacy and theability to discriminate colours. There could be tworeasons for this: (1) They live in very shallowestuaries, swamps and rivers where the availablelight is bright and probably spectrally broader thanthe coastal marine habitat encountered by the earlywhales and pinnipeds. (2) They are herbivores thatneed to discriminate fresh plants from rotten onesand from other objects, favouring the conservationof adequate colour vision (Ahnelt & Kolb, 2000).The freshwater habitats of the amphibious river

otter and hippopotamus also are shallow comparedto the coastal marine habitats encountered by earlywhales and seals, suggesting a spectrally broaderphotic environment. Furthermore, their consider-able terrestrial activities in a vegetated, spectrallyricher environment could have helped to conservecone dichromacy and colour vision. In comparison,the sandy or rocky terrain normally encountered bypinnipeds during their terrestrial activities is drab.Finally, there is an interesting parallel to sh (see,

e.g. Partridge, 1990). Many surface-living diurnalspecies of sh have several spectral cone types andgood colour visioncomparing well with the situ-ation in manatee, river otter and hippopotamus.Deeper living, but still diurnal, freshwater shespossess red cones and commonly have abandonedthe S-cones, presumably as an adaptation to theirspectral environment, as deeper freshwater, likecoastal marine water, is dominated by long-wavelight. This compares nicely with the situation pos-tulated for early whales and pinnipeds. The simi-larity vanishes for deeper living and crepuscularmarine shes, which usually possess blue and greencones, interpreted as an adaptation to the blue-shifted lighting conditions of deeper waters. Thepattern in shes again emphasizes the puzzle of the

blue cone loss in cetaceans and pinnipeds andargues for their adaptation to an early, coastalphotic environment.

OutlookThe issue of colour vision in marine mammalsremains a challenge for marine biologists andneuroscientists. More species, particularly baleenwhales, river dolphins, and the walrus have to bestudied to check the hypothesis that all whales andpinnipeds have lost their S-cones. Further behav-ioural experiments have to scrutinize the extent towhich whales and pinnipeds are able to discriminatecolours, to precisely de ne the photic conditions(mesopic or photopic) in which they can do so, andto establish the role of rods in this performance.Further molecular analyses need to show howdiVerent the deleterious mutations in the S-opsingenes actually are across species, and whether ornot there is a common basic defect in the S-opsingene control region. Molecular genetics may alsoclarify at what time points in cetacean and pinnipedevolution the S-cones were lost.

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