J Comp Physiol A (2009) 195:643–650

DOI 10.1007/s00359-009-0439-2

ORIGINAL PAPER

Aerial visual acuity in harbor seals (Phoca vitulina) as a function of luminance

Frederike Diana Hanke · Guido Dehnhardt

Received: 5 February 2009 / Revised: 19 March 2009 / Accepted: 22 March 2009 / Published online: 10 April 2009© Springer-Verlag 2009

Abstract In this study, we measured aerial visual acuityin harbor seals. As a Wrst approach to the hypothesis thatharbor seals can obtain acute aerial visual acuity mediatedby the interaction of the vertical slit-shaped pupil and thecorneal Xattening although refractive measurements hadrevealed aerial myopia, visual acuity was tested as a func-tion of luminance and pupil dilation. We analyzed aerialvisual acuity (minimal resolvable stripe width) in three har-bor seals in a two-alternative-forced-choice discriminationexperiment. Our results further support the hypothesis thatharbor seals possess an aerial visual acuity comparable tothe acuity in clear waters if the vertical slit pupil does notexceed the zone of corneal Xattening in bright light. Whenthe pupil dilates with decreasing luminance, visual acuitydecreases which might be due to deXected light from thestronger curved peripheral cornea.

Keywords Harbor seal · Phoca vitulina · Visual acuity · Luminance · Corneal Xattening

AbbreviationsIR InfraredSD Standard deviation

Introduction

The amphibious lifestyle of harbor seals (Phoca vitulina) isa challenge for all sensory systems. The most serious prob-lem of amphibious vision might be the gain in refractivepower when the eyes are lifted above the water surface.This is due to the cornea being optically nearly ineVectiveunder water but contributing large parts to the overallrefractive power of the eye in air. Harbor seals seem to beprimarily adapted for underwater vision, where essentialactivities, such as hunting, are performed. Therefore, it wasspeculated that the eye is emmetropic when immersed inwater mediated by a spherical lens (Jamieson and Fisher1972; Hanke et al. 2008) and myopic in air. Refractivemeasurements in harbor seals supported this hypothesisand, additionally, revealed a high degree of astigmatismagainst the rule, meaning that the horizontal meridian wasrefracting the light stronger than the vertical meridian(Johnson 1893, 1901; Jamieson 1970; Hanke FD et al.2006).

Interestingly, in our study on harbor seal refraction(Hanke FD et al. 2006), the degree of aerial ametropiadepended on pupil size. The high degree of aerial myopiawas measured in widely dilated pupils, however, analyzingintermediate stages of pupil constriction, vertical slits,myopia tended to decrease with decreasing vertical pupildiameter rendering the eyes near-emmetropic (Hanke FDet al. 2006). It was hypothesized that this relationship canin large be understood when looking at corneal topography(Hanke FD et al. 2006). The cornea displays a central Xatstripe with radii of curvature up to 60–80 mm in the verticalmeridian but a less pronounced Xattening in the horizontalmeridian (central radii of curvature 25–30 mm) renderingthe eye highly astigmatic. Thus, when restricting the opticalzone to the corneal Xattening by the vertical slit pupil and

F. D. Hanke (&)Department of General Zoology and Neurobiology, University of Bochum, ND 6/33, 44780 Bochum, Germanye-mail: frhanke@yahoo.de

G. DehnhardtInstitute for Biosciences, Sensory and Cognitive Ecology, University of Rostock, Albert-Einstein-Strasse 3, 18059 Rostock, Germany

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assuming emmetropia under water, the seal’s myopia couldbe reduced to approximately 4D, the diVerence in refractivepower of the central cornea between water and air. Thisvalue corresponds well to the refractions obtained in verti-cal pupil diameters smaller than the corneal Xattening(Hanke FD et al. 2006).

We hypothesize that if the vertical diameter of the slit-shaped pupil did not exceed the vertical extensions of theXat corneal stripe, the animals could obtain a high resolu-tion picture of the surroundings. In our opinion, the reducedamount of photons entering the eye is not negatively aVect-ing vision in this condition as the harbor seals’ retinae arehighly light sensitive (Walls 1942; Jamieson and Fisher1971, 1972; Peichl and Moutairou 1998; Peichl et al. 2001).However, in darkness, when the pupil fully dilates, visualacuity is expected to be worse as the emmetropic picturegenerated by the central part of the dioptric apparatus willbe deteriorated by the unsharp picture created by theperiphery and by optical aberrations related to a large aper-ture.

It has to be noted that a complete Xattening, as observedin the California sea lion (Zalophus californianus; Dawsonet al. 1987), would be even more advantageous. Up to now,there is only speculation about why in seals only onemeridian is Xattened. In our opinion, it might constitute acompromise between optical constraints in air and hydro-dynamic constraints under water (Hanke FD et al. 2006).

Walls (1942) speculated about the interaction of the ver-tical slit-shaped pupil with the corneal astigmatism for har-bor seals seeking a means of obtaining a sharp image in air.This interaction, called inactive accommodation by Sivak(1980), could result in a visual acuity better than that indi-cated by the refractive measurements, which is supportedby our own behavioral observations of good visual perfor-mance of harbor seals in air.

Aerial visual acuity in harbor seals has been analyzed byJamieson and Fisher (1970). However, as already discussedby Jamieson and Fisher (1970), their experimentalapproach, requiring the discrimination of a solid black lineversus two black lines separated by a gap, seem to havetested absolute sensitivity of the eye rather than visual acu-ity. As of now, there are two studies presenting reliable datafor aerial visual acuity in pinnipeds, the California sea lion(Zalophus californianus; Schusterman and Balliet 1971)and two species of fur seals (Arctocephalus pusillus andArctocephalus australis; Busch and Dücker 1987). How-ever, the transfer of the acuity data of the California sealion (Schusterman and Balliet 1971) to harbor seals seemsimpossible. This is due to the fact that the cornea of the sealion displays a completely, in both meridians, Xat windowon the cornea (Dawson et al. 1987). The data on fur seals(Busch and Dücker 1987) can neither be applied because nodata on corneal topography in these species is available and

because the acuity data have been obtained in uncontrolledlight conditions.

The purpose of this study was to gain missing but highlyimportant data on the resolution capacity of harbor seals’eyes in air. Visual acuity was determined under six diVerentlight conditions ranging from 0.15 cd/m2 up to 80 cd/m2 inorder to assess how aerial visual acuity is limited by lumi-nance. We monitored pupil diameter during all experimen-tal sessions as a Wrst approach to the hypothesis of aninteraction of the slit-shaped pupil with corneal topographymediating aerial visual acuity. We measured visual acuityin three harbor seals psychophysically as the minimalresolving stripe width using black-and-white gratingswhich is considered a reliable technique for studying visualacuity (Rahmann 1967).

Materials and methods

Experimental animals

The visual acuity experiments were carried out at theMarine Science Center (http://www.msc-mv.de), Germany.We tested three out of a group of eight male harbor seals,Phoca vitulina (“Enzo”, 3 years old; “Bill”, 6 years old;“Sam”, 13 years old). During the current experiments, theoptical status of the seals’ eyes was perfect for “Enzo”who has never had any eye infections. “Bill’s” eyesalmost constantly and also during these visual acuityexperiments display a slight corneal cloudiness, and“Sam’s” eyes were perfect during the whole time of datacollection but his corneae show permanent irregularitiesfrom former corneal infections. All animals had experi-ence with visual experiments. “Bill” and “Sam” hadalready taken part in a study on underwater visual acuity(WeiVen et al. 2006), “Enzo’s” and “Sam’s” refractionhad been obtained in air, and data on corneal topographyin “Enzo” are available (Hanke FD et al. 2006). Exceptfor “Bill”, all seals were highly adapted to work in a darkchamber.

Approximately 90% of the daily amount of food (1.5–4 kg of herring depending on age, season, and motivation)was given to the seals during experiments which were con-ducted once or twice per day 5–7 days per week.

Experimental setup

Measurements were carried out in an experimental cham-ber. At the front side of the chamber, a white stimulusboard was installed (Fig. 1a, b). It consisted of two pocketsallowing the insertion of the gratings on the backside and amovable cover on the front side. The whole front side of thechamber was additionally Wt out with white linen in order to

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illuminate the animal’s visual Weld homogenously. Theexperimenter could hide entirely behind the stimulus boardand the white linen. A small window (size 100 £ 100 mm)was cut in the white linen to be able to reward the animalaccording to its behavior. The experimenter could observethe animal through the rewarding window via a small mirror.The animal rested at a stationary target at a distance of60 cm from the stimulus board (Fig. 1b). We Wt a ring to thestationary target in order to assure a comparable head posi-tioning over trials and sessions. Two 10 cm plastic spheres,one to the animal’s right and one to its left, served asresponse targets.

Stimuli

Visual acuity was determined as the minimal resolvablestripe width. Stimuli consisted of black-and-white stripepatterns with deWned stripe widths. Contrast deWned as(Lmax ¡ Lmin)/(Lmax + Lmin) with Lmax and Lmin being theluminance of the white and black bars, respectively wasmeasured with a Minolta LS-110 luminance meter and was0.86 § 0.01 under all values of ambient luminance. Thestimuli had already been used for underwater measure-ments of visual acuity and were described in detail inWeiVen et al. (2006). Stimuli were presented pair wise(Fig. 1a) which means that a horizontal stripe pattern withdeWned stripe width and a vertical stripe pattern with thesame stripe width were presented to the animal simulta-neously. With this experimental approach, the overallbrightness of both stripe patterns was identical, thus theanimal could not rely on brightness cues for making its

decision. The animal’s task was to indicate the position ofthe positive stimulus (horizontal grating) in a two-alterna-tive-forced-choice discrimination. Measuring visual acuityat a viewing distance of 60 cm (Fig. 1b) one stripe patternextended over 18° £ 18° in the animal’s visual Weld. As thegratings were separated by 20 cm (Fig. 1a), the outer bor-ders of the gratings were viewed under an angle of 52°which is well within the binocular visual Weld of harborseals (Hanke W et al. 2006). We presented stripe widthsranging from 0.5 to 8 mm using the method of constantstimuli. To measure visual acuity under the lowest lightcondition, we tested stimulus pairs with stripe widths rang-ing from 0.75 to 9 mm to assure that the animal had to dealwith only few stimulus pairs below threshold, which was aprerequisite for a high motivation level.

Ambient luminance

Experiments were carried out in an experimental chamberto be able to adjust ambient luminance. We measuredvisual acuity in six diVerent light conditions: 0.15, 4.5, 23,43, 63, and 80 cd/m2. These values refer to the mean lumi-nance in four locations within the animal’s visual Welds,including the two gratings and one Weld on the white linento the animal’s left and one to its right side. For illumina-tion, four halogen lamps (25 W) were positioned behind theanimal to avoid blinding. Two lamps were placed on bothsides of the animal, two lamps above its head (Fig. 1a).With the help of a dimming device, the brightness of thelamps could be set to the desired value (accuracy § 3 cd/m2

at high luminance). Luminance was determined with the

Fig. 1 Experimental setup to test visual acuity as a function of lumi-nance in harbor seals. a Frontal view. b Side view. Stimuli [black-and-white stripe patterns with the horizontal grating as the positive stimulus(PS) and the vertical grating as the negative stimulus (NS)] were pre-sented pair wise on a white board separated by 20 cm and only becamevisible for the seal when a movable cover (CV) was lifted. The seal wasstationing in a hoop station 60 cm in front of the board and made itsdecision by moving the head to one of two response targets (RT), oneto the left and one to the right. Four halogen lamps (L1–L4), two above,

one to the left and one to the right side of the seal, homogenously illu-minated the visual Weld of the seal, which was Wt out with white linen.The camera (C) constantly Wlming the seal’s left eye in order to be ableto monitor pupillary dilation was installed slightly to the left of thestimulus board. The experimenter hid behind the stimulus board andwhite linen and could observe the seal’s response via a small rewardingwindow (RW) cut into the white linen and a mirror (M). The Wshreward was delivered through the small rewarding window (RW)

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help of a luminance meter (see “Stimuli”). It is important tonote that luminance is a photometric unit based on thehuman spectral sensitivity.

Monitoring and analysis of pupil diameter

Pupil diameter was monitored and recorded during all ses-sions. For this purpose, a monochrome CCD camera (DMK2002, The Imaging Source, Bremen, Germany) wasinstalled directly at the side of the left grating (Fig. 1a)which Wlmed a close up of the left eye of the animal contin-uously. Measurements were along the optical axis of theeye. If ambient luminance was low, we used additionalinfrared (IR)-light to obtain analyzable pictures of theseals’ eyes. For converting pupil diameter to millimeter, weattached a white paper dot with a diameter of 8 mm actingas a scale next to the animal’s left eye. All video recordingswere digitized and exported into single frames. For analy-sis, we measured the vertical and horizontal pupil diameter.One measurement was made for each trial resulting in 60measurements per session.

Procedure

At the beginning of each session, the animal was calledinside the chamber and guided to the stationing target. Thescale (see “Monitoring and analysis of pupil diameter”) wasattached next to the animal’s eye, and the camera’s positionwas adjusted to optimize the quality of the video record-ings. The experimenter then hid herself completely behindthe stimulus board and white linen. The video recordingwas started, and the Wrst stimulus pair was inserted behindthe cover. After 5 s, the cover was lifted which served as astart signal for the animal to make its decision. If the posi-tive stimulus (horizontal grating) appeared on the left, theanimal had to touch the response target to the left with itssnout for a correct choice and vice versa. After a correctchoice, the seal was rewarded with a piece of herring. If itresponded incorrectly, its response was answered verballywith “no”. In both cases, after the reward or after the “no”signal, the animal stationed at the stationing target againand remained there until the next trial started. The coverwas lowered, and the stimulus pair was changed in accor-dance with a pseudo-randomized scheme (Gellermann1933).

Before starting data collection, each seal was required torespond with a performance of more than 90% correctchoice to stimuli well above threshold for at least Wve con-secutive sessions. All in all, 30 sessions were required for acomplete data set for each seal after the seals’ performancehad reached the criterion. During these 30 sessions, each ofthe six values of ambient luminance was tested Wve times.Luminance values were changed in a random order over

sessions. Each of the stimulus pairs was shown to the sealsix times per session resulting in 30 presentations per stim-ulus pair per ambient luminance.

Analysis of psychometric functions

Visual acuity was deWned as the visual angle of the stripewidth the seal could detect with 75% correct choice at a dis-tance of 60 cm. It was determined by linearly interpolatingbetween the stripe width just under threshold and the stripewidth just above threshold. Thresholds were converted tovisual angles as visual angle = arctan (threshold stripewidth/viewing distance).

Results

All results for the three harbor seals including ambientluminance, visual angles and horizontal and vertical pupildiameters with standard deviations (SD) are listed inTable 1. Figure 2 represents the results graphically, plottingvisual angle and the ratio of pupil diameters (horizontalpupil diameter/vertical pupil diameter) as a function of thesix levels of ambient luminance for all tested seals sepa-rately (Fig. 2a–c) and as mean values (Fig. 2d; error barsindicate the SD).

The minimum acuity values determined for the threeseals lie in the range of 5.3�–6.3� (mean value § SD:5.6� § 0.6� or 5.4 § 0.5 cycles/deg). These values wereassessed at the highest ambient luminance adjusted to80 cd/m2 except in seal “Sam” whose acuity was better by2� at 63 cd/m2. With decreasing ambient luminance, visualacuity decreases. Considering the minimum and maximumacuity value for each seal, acuity decreases by a factor of2–3 in the measured range. The decrease is pronouncedbelow approximately 25 cd/m2. At the dimmest luminanceof 0.15 cd/m2, visual acuity ranges from 10.9� to 16.1�

(mean value § SD: 13.8� § 3.7� or 2.2 § 0.5 cycles/deg).Generally, the acuity values at an ambient luminance of43 cd/m2 deviate from the otherwise smooth acuity func-tion in all seals (Fig. 2a–c). Acuity at this luminance isworse than the general function would predict and seems tobe out of range in seal “Enzo” even after replication.

The pupil dilates constantly with decreasing ambientluminance (Table 1, Figs. 2, 3). Figure 3 illustrates thiseVect in form of single frames obtained by digitizing thevideo recordings of the camera monitoring pupillarydilation for seal “Sam”. Over a broad range of high lumi-nance values, the pupil stays constricted as a vertical slitwith only slight changes in diameter. Although the pupildiameters stay almost constant, visual acuity slightlydecreases with decreasing ambient luminance. Belowapproximately 25 cd/m2, when visual acuity drastically

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decreases, the pupil is markedly dilated (Figs. 2, 3). Var-iability in pupil diameter is generally low (Table 1).Interestingly, the pupils of the three seals react diVer-ently to light of the same brightness. Whereas both pupildiameters of the eyes of the seals “Enzo” and “Bill”dilate by mean values of 2.6 and 2.4 mm, respectively,both pupil diameters in the seal “Sam” increase by amean value of 7.6 mm.

Discussion

In this study, we measured aerial visual acuity in three har-bor seals as the minimal resolvable stripe width as a func-tion of luminance. During the experiments, pupil dilationwas constantly monitored in order to obtain further infor-mation concerning the hypothesis of an interaction of theslit-shaped pupil with the corneal Xattening.

Table 1 Results of visual acuity experiments indicating the experimental animal, ambient luminance (in cd/m2), mean horizontal and vertical pupil diameter (in mm § SD) and visual acuity angle (in min)

Experimental animal

Ambient luminance (cd/m2)

Horizontal pupil diameter (mm) and SD

Vertical pupil diameter (mm) and SD

Visual acuity angle (min)

Enzo 80 0.88 § 0.15 3.75 § 0.34 5.27

63 0.87 § 0.15 3.83 § 0.28 5.64

43 0.90 § 0.15 3.77 § 0.28 12.41

23 1.14 § 0.17 4.10 § 0.24 8.59

4.5 1.89 § 0.26 4.88 § 0.24 13.05

0.15 3.27 § 0.42 6.49 § 0.33 16.11

Bill 80 1.14 § 0.21 4.37 § 0.33 5.30

63 1.19 § 0.18 4.25 § 0.37 5.66

43 1.34 § 0.21 4.53 § 0.29 7.96

23 1.76 § 0.20 4.94 § 0.31 7.32

4.5 2.56 § 0.36 5.84 § 0.39 8.12

0.15 3.44 § 0.30 6.93 § 0.18 10.88

Sam 80 1.36 § 0.10 4.90 § 0.16 8.36

63 1.32 § 0.18 5.05 § 0.26 6.30

43 1.43 § 0.23 5.08 § 0.30 8.79

23 2.21 § 0.42 6.09 § 0.66 8.07

4.5 3.66 § 0.95 7.71 § 1.02 10.50

0.15 9.12 § 1.08 12.34 § 0.86 14.32

Fig. 2 Results of visual acuity experiments. Visual angles (in min of arc) and the ratio of pupil diameters (horizontal pupil diameter/vertical pupil diame-ter) are presented as a function of ambient luminance (in cd/m2) for the three seals separately (a “Enzo”, b “Bill”, and c “Sam”) and as d mean values of the individual data with SD. Open triangles visual angle, Wlled dots ratio of pupil diameters

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It has to be noted that, testing visual acuity with gratings,spurious resolution might have occurred if defocus was thelimiting factor resulting in an overestimation of visual acu-ity. However, even if visual acuity was overestimated, theinXuence of luminance on visual acuity could still beassessed. Furthermore, with this approach, it was possibleto compare our results with those of other studies that hadall tested visual acuity with acuity gratings.

Our data indicate that in bright light conditions (20–80 cd/m2), harbor seals can rely on a visual acuity in air thatcompares well with the acuity found when the eyes areimmersed in clear and bright waters (Schusterman and Bal-liet 1970; WeiVen et al. 2006) and with the acuity valuesassessed in other pinnipeds (Schusterman and Balliet 1970,1971; Busch and Dücker 1987) and in many terrestrialmammals (Rahmann 1967). From the results of this studyand of several studies which revealed good resolution of theseals’ eyes under water (Johnson 1893, 1901; Walls 1942;Jamieson 1970; Schusterman and Balliet 1970; Hanke FDet al. 2006; WeiVen et al. 2006), we conclude that a solu-tion to the main problem of amphibious vision evolved inharbor seals’ eyes concerning bright light conditions.

In these bright light conditions, the seals’ pupils adoptthe form of small vertical slits. Taken the data on cornealtopography of seal “Enzo”, these small slits do not exceedthe vertical extensions of the Xat corneal stripe (Hanke FDet al. 2006). This experimental Wnding together with theresults of refractive measurements outlined in the “Intro-duction” lends further support to the hypothesis of an inter-action of the vertical slit pupil with the Xat corneal striperesulting in good aerial visual acuity. Interestingly, theseals’ pupils stay constricted as vertical slits smaller thanthis corneal Xattening over a broad range of the ambientluminance range we used in this study. Visual acuity mightbe optimized by this pupil shape comparable to humans inwhom visual acuity is optimized by a certain pupil shape

over a wide range of luminance levels balancing diVractionand optical aberrations (Woodhouse 1975).

The visual acuity values obtained in bright light are in thesame order of magnitude as the retinal resolution obtained inthree pinniped species in air (3.6�–7.1�; Mass and Supin1992, 2003, 2005). Our own unpublished data on ganglioncell topography in harbor seals (Hanke et al. unpublisheddata) revealed a retinal resolution of 3.5� in air based on thetotal ganglion cell density. However, visual acuity is deter-mined only by the ganglion cells with the smallest receptiveWelds, the beta ganglion cells (for review see Wässle 2004).If the beta ganglion cells comprise 50% of the total ganglioncell population in harbor seals as they do in cats (Wässle2004), retinal resolution is calculated as 4.9� in air. Thisvalue is close to the behaviorally assessed visual acuity inbright light. Consequently, the optics is limiting the resolu-tion of the harbor seal eye only to a small extent if thebehavioral visual acuity was not overestimated by e.g., spu-rious resolution. The interaction of the slit pupil with thecorneal Xattening could reduce aerial myopia to 4D assum-ing emmetropia under water (see “Introduction”). Thus, theseal would need just small amplitude of accommodation, forwhich we have Wrst indication (Hanke FD et al. 2006), toachieve the good aerial resolution taking into account thatthe seal could have been even up to 1.7D myopic to resolvethe grating at a viewing distance of 60 cm.

In accordance with the results of this study, we think thatthe high degree of myopia obtained in refractive measure-ments (Johnson 1893, 1901; Hanke FD et al. 2006) doesnot represent the general refractive state of harbor seals’eyes but reXects a methodological problem. In IR-photore-tinoscopy (SchaeVel et al. 1987; for application on harborseals see Hanke FD et al. 2006), the IR-light of the IR-pho-toretinoscope enters the eye, is partly reXected by the ocularfundus and elicits a brightness distribution in the widelydilated pupil. The slope of this brightness distribution can

Fig. 3 Results of pupillometry. One example frame obtained with the camera monitoring the left eye of seal “Sam” illustrat-ing the dilation of the pupil for each value of luminance: 80, 63, 43, 23, 4.5, 0.15 cd/m2. Note that the pupil stays constricted as a vertical slit over a broad range of ambient luminance. Scale bar 5 mm

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be converted into refraction. In harbor seals, the brightnessdistribution adopts an s-shaped form which suggests thepresence of a large amount of higher order aberrations.These need to be determined in detail by a Hartman–Shackwavefront sensor. However, the s-shaped brightness proWlemight mirror corneal topography with a central “plateau”corresponding to the Xat corneal stripe (Hanke FD et al.2006). The high degree of myopia was assessed by averag-ing the slope of the brightness proWle obtained in the wholeaperture which is the common procedure. However, inthese conditions the information of this s-proWle is lost, andthus, assuming that it reXects the corneal Xattening, the spe-ciWc corneal topography would not be taken into account.Ametropia is drastically reduced if, by artiWcially shorten-ing the brightness proWles, only the central “plateau” is ana-lyzed, which produces an error because all points on theretina act as diVuse reXectors and contribute to every pointof the brightness proWle. Ametropia is also reduced ifrefractive measurements are performed with pupil sizesvertically smaller than the Xat corneal stripe. In line withthe results of this study, harbor seals might indeed possessan emmetropic picture if the pupil is small enough, and thataveraging the refraction over corneal parts with diVerentcurvature in dilated pupils would feign myopia. Using clas-sic retinoscopic methods applied on harbor seals by John-son (1893, 1901) and by Jamieson (1970), a high degree ofametropia could result if measurements were oV-axis notscanning the central picture but instead assessing refractivestate through the stronger refracting periphery. Addition-ally, if repeated measurements were performed along diVer-ent optical axes, the speciWc corneal topography could alsoexplain some of the variability Jamieson (1970) faced dur-ing his refractive measurements.

In our experiments, visual acuity decreases with decreas-ing ambient luminance. The loss of acuity is pronouncedbelow an ambient luminance of approximately 25 cd/m2

and is accompanied by a marked increase of both pupildiameters. Therefore, the decline in visual acuity might beexplained by optical factors related to pupil size. In awidely dilated pupil, light rays entering the eye are alsorefracted by the stronger curved peripheral cornea (HankeFD et al. 2006). Assuming that an image close to emmetro-pia is generated by the light entering the eye through thecentral parts of the pupil, this image will be overlaid byunfocused light from the periphery which will impair visualacuity. However, further studies are needed in order toassess the inXuence of other factors, such as higher conver-gence of the rods compared to the cones along with a shiftfrom photopic to scotopic vision, on visual acuity in dimlight.

The brightness range we used in this study to measurevisual acuity covers approximately one logarithmic unitwhich is only a small section of the brightness spectrum

met under natural conditions, approximately 10 logarithmicunits (Land and Nilsson 2002). However, the range we usedserved to elicit various degrees of pupillary dilation fromwidely, almost circularly dilated to small vertical slits andwas adjusted to obtain further insight regarding the interac-tion between pupillary opening and Xat corneal stripe con-cerning visual acuity. In light conditions much brighterthan our brightest condition, the pupil closes to a pinhole,and visual acuity might be better than the best acuity valueswe obtained in this study because the pinhole eVect mini-mizes all deleterious eVects, as e.g., the cornea’s astigma-tism (Hanke FD et al. 2006) and all aberrations related to abig aperture. The fact that the amount of photons enteringthe eyes relative to bigger pupils is probably drasticallyreduced in the pinhole situation is, as already discussed,expected to be negligible in seals. Under light conditionslower than our dimmest luminance, we would expect thatharbor seals’ visual acuity would further decrease due toincreased noise related to low photon numbers.

To conclude, the harbor seal eye seems to possess goodresolution in air and water in bright light conditions. It isassumed to be highly adapted for amphibious vision. Con-cerning aerial vision, the present study presents further evi-dence that the good resolution might be achieved by theinteraction of the slit pupil with the corneal Xattening.

Acknowledgments The authors would like to thank Christine Schol-tyssek and Wolf Hanke for critically reading the manuscript. Thisstudy was supported by a grant of the Studienstiftung des DeutschenVolkes (2005 SA 0969) to FDH and grants of the VolkswagenStiftungand the Deutsche Forschungsgemeinschaft (SFB 509) to GD. Theexperiments were in line with the current German law on the protectionof animals.

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