ORIGINAL PAPER

Contrast sensitivity in a harbor seal (Phoca vitulina)

Frederike D. Hanke • Christine Scholtyssek •

Wolf Hanke • Guido Dehnhardt

Received: 31 July 2010 / Revised: 29 September 2010 / Accepted: 9 October 2010 / Published online: 28 October 2010

� Springer-Verlag 2010

Abstract In this study, the contrast sensitivity function

(CSF) of one harbor seal was determined behaviorally in a

go-/no-go-experiment at an ambient light of 0.9 lx in air.

Contrast sensitivity was assessed as the reciprocal value of

the threshold contrast for spatial frequencies varying

between 0.03 and 1.5 cycles/deg, which were displayed

with contrast ranging from 0.02 to 1 on a TFT monitor with

a mean luminance of 3.8 cd/m2. The CSF of the harbor seal

shows the general characteristics described for other spe-

cies with a peak at an intermediate frequency, a low fre-

quency roll-off and a high frequency cut-off towards the

harbor seal’s resolution limit determined in a previous

study. The position of the CSF’s peak lies at approximately

0.5 cycles/deg and adopts an absolute height of 40. These

results compare well with the cat’s CSF assessed at a

comparable adaptation light which might reflect similari-

ties in lifestyle and optics.

Keywords Harbor seal � Phoca vitulina � Vision �Contrast sensitivity � Resolution

Introduction

Contrast sensitivity is defined as the lowest contrast an

organism can detect for a given target size. Thus, contrast

sensitivity takes two parameters into consideration, con-

trast and spatial frequency. Consequently, contrast sensi-

tivity testing extends the assessment of visual function

beyond visual acuity and brightness discrimination. It is

often called ‘‘functional vision’’ or ‘‘real-world visual

performance’’ (Woods and Wood 1995) because it gives a

better estimate of the visual abilities of an organism. This is

due to the fact that the detection and identification of an

object varies with its size, contrast and spatial orientation

(Olzak and Thomas 1986). It has been demonstrated that

contrast sensitivity, not visual acuity, predicts how well

subjects see real-world targets or everyday objects (Gins-

burg et al. 1982; Owsley and Sloane 1987).

Among marine mammals, the vision of pinnipeds, in

particular the visual system of harbor seals, is best

described (Jamieson and Fisher 1972; Kroger and Katzir

2008; Reuter and Peichl 2008; Hanke et al. 2009a). In

previous studies on the visual system of harbor seals, visual

acuity (Schusterman and Balliet 1970; Weiffen et al. 2006;

Hanke and Dehnhardt 2009) and brightness discrimination

abilities (Scholtyssek et al. 2008) were assessed. However,

no data are available regarding contrast sensitivity for any

marine mammal.

Contrast sensitivity is of special interest in aquatic or

amphibious carnivores because their lifestyle requires the

detection of differently sized objects, such as prey fishes

from the background. This is challenging in the underwater

environment because under many circumstances, the con-

trast between object and background is low. This is par-

ticularly true when a seal feeds on benthic prey, which is

often cryptic. Contrast under water is often inherently

reduced to a large extent because light reflected from

objects is mostly similar to the background light due to

scattering and absorption (Duntley 1963; Warrant and

Locket 2004; Cronin 2006; Kroger 2008). Light that

reaches the object is scattered and absorbed both on the

way to the object and from the object to the observer.

Veiling light further degrades the visibility of objects. In

F. D. Hanke (&) � C. Scholtyssek � W. Hanke � G. Dehnhardt

Institute for Biosciences, Sensory and Cognitive Ecology,

University of Rostock, Albert-Einstein-Strasse 3,

18059 Rostock, Germany

e-mail: frhanke@yahoo.de

123

J Comp Physiol A (2011) 197:203–210

DOI 10.1007/s00359-010-0600-y

harbor seals, it was shown that turbidity can severely

impair underwater vision even in bright light (Weiffen

et al. 2006).

Under many circumstances, light is already limited in air

as well as under water. Harbor seals experience low

luminance or even darkness when diving to greater depths

during the day, when most of the daylight is reflected at the

water surface and only a fraction of light penetrates the

water, or when foraging or navigating at dusk, dawn or at

night. Low ambient luminance reduces the visibility of

objects. Therefore, adaptations that enhance contrast sen-

sitivity are important, since they expand the volume of

observable space in an animal’s aerial and underwater

habitat that can be sampled for prey, predators, competitors

or conspecifics and for orientation.

Adaptations for dim light vision and for the enhance-

ment of contrast are present at the behavioral level. For

example, several pinniped species have been reported to

silhouette their prey against the bright water surface

(Hobson 1966; Davis et al. 1992, 1999). However, adap-

tations primarily reside in the eye itself (Hanke et al.

2009a), and in the way visual information is processed and

perceived. In the present study, we determined the contrast

sensitivity function (CSF) of one harbor seal in a beha-

vioral experiment as an approach to the question of how the

perception of a range of spatial frequencies varies with

contrast in dim light in an amphibious mammalian carni-

vore. We thus assessed the seal’s functional vision in air

complementing the previous studies on brightness dis-

crimination and on visual acuity (Scholtyssek et al. 2008;

Hanke and Dehnhardt 2009).

Materials and methods

Contrast sensitivity was measured in a 15-year-old male

harbor seal (Phoca vitulina) at the Marine Science Center,

Germany (http://www.msc-mv.de). The animal had already

participated in a number of visual experiments (Hanke FD

et al. 2006; Hanke W et al. 2006; Weiffen et al. 2006;

Hanke et al. 2008b; Hanke and Dehnhardt 2009).

The experimental setup used for contrast sensitivity

measurements in this study is shown in Fig. 1. Contrast

sensitivity was assessed in air in an experimental chamber

(4 m 9 2 m 9 2 m) in which the illumination could be

adjusted to 0.9 lx (equivalent to a luminance of 0.5 cd/m2

measured with a luminance meter, LS-110, Konica-

Minolta). Details about the illumination are described in

greater detail elsewhere (Scholtyssek et al. 2008). The

stimuli were displayed on an 18 in. TFT monitor (FlexScan

L685, Eizo), which was installed in a stimulus board

(1.5 m 9 1.2 m). This board also served to hide the

experimenter to avoid secondary cueing. Stimuli consisted

of sinusoidal gratings generated in Matlab (The Math-

works, Natick, Massachusetts, USA) with spatial frequen-

cies ranging from 0.03 to 1.5 cycles/deg. We focused our

contrast sensitivity testing on spatial frequencies below

2 cycles/deg because the experimental animal’s resolution

maximum had already been determined as 2.9 cycles/deg

in ambient luminance of 4.5 cd/m2 and as 2.1 cycles/deg in

ambient luminance of 0.15 cd/m2 in a prior study (Hanke

and Dehnhardt 2009). The spatial frequencies were dis-

played with contrasts ranging from 0.02 to 1. Contrast was

defined as the Michelson’s contrast C = (Lmax – Lmin)/

(Lmax ? Lmin), where Lmax is the maximum luminance and

Lmin the minimum luminance of the gratings. The spatial

frequencies were tested against a uniform gray stimulus

with the mean luminance of the gratings (3.8 cd/m2). The

mean luminance of the gray reference field was matched to

the mean luminance of the grating based on the pixel

50 cm

M

RTST

M

50 cmST

RT

a

b

SP

SP

IB

Fig. 1 Experimental set-up for contrast sensitivity measurements.

Measurements were performed in a chamber to be able to adjust

luminance to 0.9 lx with the help of an illumination box, which was

mounted above the experimental setup. Stimuli were displayed on a

TFT monitor that was inserted in a stimulus board at a distance of

50 cm from the seal. The stimulus board also served to hide the

experimenter, who could observe the animal via a small mirror to

reward the animal according to its behavior. Contrast sensitivity was

tested in a go-/no-go-paradigm with a vertical stripes with variable

spatial frequency and variable contrast as go-stimuli, animal moves its

head to a response target to its right, and b a homogenously graydisplay as the no-go stimulus, animal has to stay at the stationing

target for a 3 s time interval. A slide plate hid the stimuli between

trials when the next stimulus was generated. IB illumination box,

M mirror, RT response target, SP slide plate, ST stationing target

204 J Comp Physiol A (2011) 197:203–210

123

values. Luminance measurements of the monitor showed

that luminance was related to pixel values sufficiently

linearly between pixel values of 100–150 so that the seal

could not use brightness cues to discriminate the grating

from the gray reference field based on the brightness dis-

crimination thresholds for harbor seals (Scholtyssek et al.

2008). Adopting such a strategy would further be compli-

cated by the fact that in the present study, the stimuli were

presented in sequence rather than as a forced choice

paradigm.

During data recording, we had to introduce noise to be

able to assess a contrast threshold for certain spatial fre-

quencies. At these spatial frequencies, contrast thresholds

lay below 0.02. However, with our technical equipment, the

presentation of contrasts below 0.02 led to artefacts; the

gratings were displayed with a stepwise change in brightness

instead of sinusoids with a gradual change in brightness. By

testing these spatial frequencies in noise, the contrast

thresholds were shifted to values within the displayable

range. For contrast sensitivity testing in noise, a matrix of the

width of the grating (1,280 9 1,024 pixel) of random gray

values was added to the display. The gray values of the noise

were normally distributed around zero with a standard

deviation of 0.6 times the mean pixel value of 127.

Contrast sensitivity was tested in a behavioral experi-

ment using a go-/no-go-paradigm (Fig. 1). The seal was

stationed in a ring station 50 cm from the monitor. Thus,

the stimulus display extended over 37.6 deg of visual angle

which is well within the binocular visual field of harbor

seals (Hanke W et al. 2006). Prior to each experimental

trial, the monitor was covered by an opaque slide plate.

A trial was initiated by lifting this plate so that the seal

could see the stimulus. When presented with a grating, the

go-stimulus, the seal was required to leave the station and

put its snout on the response target to its right within 3 s

(Fig. 1a). When the uniform gray stimulus was shown, the

no-go-stimulus, the seal had to stay at its station for at least

3 s (Fig. 1b). The response of the seal could be viewed via

a small mirror, and the seal was rewarded with a piece of

herring according to its behavior.

Initially, the seal was trained on the go-/no-go-paradigm

with a gray card presented against a card with black and

white stripes of 30 mm width, which were familiar to the

seal from the previous visual acuity experiment (Hanke and

Dehnhardt 2009). After six sessions, the seal’s performance

was greater than 90% correct. We continued training until

eight sessions above 90% correct were achieved before we

introduced the monitor and tested gray against a sinusoidal

grating (spatial frequency 0.4 cycles/deg, contrast 1). After

reaching a performance level above 90% after five ses-

sions, we generalized on spatial frequency and contrast.

The seal always had to stay above 90% correct choices for

at least five sessions, and had to answer with low false

alarm rates, defined as percent go-response to no-go-stim-

uli, before a new training step was initiated. Data collection

was started after successful generalization training.

During data collection, the contrast threshold was

determined for each spatial frequency. To obtain the psy-

chometric function, and thus the contrast threshold at a

certain spatial frequency, six contrasts were shown to the

seal 30 times each over several sessions (method of con-

stant stimuli). The subject was presented with slightly more

contrasts above the contrast threshold than below the

contrast threshold at each spatial frequency to assure a high

motivation level. The contrasts tested per spatial frequency

were chosen according to the seal’s performance during

training. During data collection, several spatial frequencies

were simultaneously tested in one session. One session

consisted of 60–120 presentations with 50% go- and 50%

no-go-stimuli presented in pseudorandom order (Geller-

mann 1933).

The contrast threshold was defined as the Michelson

contrast of the sinusoidal grating at which the seal per-

formed 50% correct choices. The contrast threshold was

determined by fitting the psychometric function with a

sigmoidal function (SigmaPlot 10.0, Systat Software Inc,

San Jose, CA, USA). Contrast sensitivity could then be

calculated as the reciprocal value of the threshold contrast

needed to identify the vertical stripes.

Results

The psychometric functions obtained at all tested spatial

frequencies are shown in Fig. 2. They represent the hit rate

defined as percent correct response to go-stimuli as a

function of contrast. The contrast thresholds could be

obtained from the psychometric functions by sigmoidal fits

with high correlation coefficients (r2 = 0.91–1). They are

presented as the CSF, i. e. the contrast sensitivity as a

function of spatial frequency in a double logarithmic plot

(Fig. 3).

We obtained contrast thresholds for all spatial frequen-

cies except for 0.3 and 0.7 cycles/deg. At these spatial

frequencies, our experimental animal performed at 60%

correct choices at 0.3 cycles/deg and at 70% correct

choices at 0.7 cycles/deg when the respective spatial fre-

quency was presented with a contrast of 0.02 (Fig. 2a),

which was the lowest contrast that could be displayed

without artefacts. To obtain contrast thresholds for these

spatial frequencies, we tested the spatial frequencies at the

CSF’s maximum, 0.3, 0.5, and 0.7 cycles/deg, additionally

in noise (Fig. 2b).

Noise and non-noise measurements (Fig. 3a) were fused

under the assumption that contrast sensitivity decreases by

a constant value across the respective range of spatial

J Comp Physiol A (2011) 197:203–210 205

123

frequencies when noise is added. This assumption is based

on the experimental findings in humans (Nordmann et al.

1992), who found that a relatively small, but consistent

decrement occurred across a wide range of spatial fre-

quencies in the middle part of the CSF. Thus, we calculated

the difference between the noise and non-noise value

determined at 0.5 cycles/deg, and shifted all noise mea-

surements by this calculated difference. This procedure is

assumed to be the best approximation of the contrast sen-

sitivity values at the maximum of the seal’s CSF for which

we have the qualitative behavioral assessment that they are

higher than the contrast sensitivity of 39 assessed at

0.5 cycles/deg.

The contrast sensitivity data were further analyzed for

cross-species comparison following Uhlrich et al. (1981)

(see Fig. 3b). The data were normalized to a proportion of

0

10

20

30

40

50

60

70

80

90

100

10.10.01

contrast

pe

rfor

man

ce (

%)

0.03

0.05

1.50.08

0.1

10.2

0.7

0.3

0.5

0

10

20

30

40

50

60

70

80

90

100

10.10.01

contrast

pe

rfor

man

ce (

%)

0.3

0.70.5

a

b

Fig. 2 Psychometric functions of contrast sensitivity measurements.

a Psychometric functions obtained at eight spatial frequencies ranging

from 0.03 to 1.5 cycles/deg. b Psychometric functions obtained from

contrast sensitivity measurements in noise at the spatial frequencies of

0.3, 0.5, 0.7 cycles/deg. The performance of the harbor seal (hit rate

in %) is plotted as a function of contrast (logarithmic scale) for each

spatial frequency. The spatial frequencies (in cycles/deg) are

indicated at the psychometric functions. Contrast sensitivity was

calculated with the help of the contrast threshold defined as the

contrast at which the seal performed 50% correct choices

1

10

co

ntra

st s

ensi

tivity

0.01

0.1

1

norm

aliz

ed c

ontr

ast s

ensi

tivity

b

-4

100a

spatial frequency (cycles/deg)

octave distance from peak

43 210-1-2-3

0.1 1

Fig. 3 Contrast sensitivity function (CSF) of a harbor seal. a Contrast

sensitivity (reciprocal value of the contrast threshold at the respective

spatial frequency) is plotted as a function of spatial frequency (in

cycles/deg) in a double logarithmic plot. Open circles represent the

values obtained during the general contrast sensitivity measurements,

filled circles represent the values of the contrast sensitivity measure-

ments in noise. b CSF of a harbor seal after fusion of noise and non-

noise measurements and normalization of contrast sensitivity values

to a proportion of the sensitivity maximum. Spatial frequency is

expressed as octave distance from the peak. The data were fit with the

function S(c) = 100(K1e-2pac - K2e-2pbc) with S(c) the contrast

sensitivity for spatial frequency c (Uhlrich et al. 1981). Arrowsindicate the maximum cut-off frequency determined in a previous

experiment on aerial visual acuity (Hanke and Dehnhardt 2009) as

2.9 cycles/deg in light of 4.5 cd/m2 (right arrow) and as 2.1 cycles/

deg in light of 0.15 cd/m2 (left arrow)

206 J Comp Physiol A (2011) 197:203–210

123

the peak contrast sensitivity, and spatial frequency was

expressed as octave distance from the peak. The best fit

with the function S(c) = 100(K1e-2pac - K2e-2pbc) with

S(c) the contrast sensitivity for spatial frequency c was

obtained with K1 = 0.8061, K2 = 0.8077, a = 0.3542,

b = 0.3658 with a goodness of fit defined as the average

squared deviation between predicted value and actual score

of 0.0159. The peak of this transformed CSF was localized

at 0.47 cycles/deg with a peak contrast sensitivity of 0.90.

The CSF of our harbor seal has a width at half amplitude of

approximately 3.22 octaves.

In general, the seal’s responses were reliable. False

alarm rates varied between 0 and 20%

(mean = 7.3 ± 4.7%) for contrast sensitivity testing

without noise. When noise was introduced, the seal’s false

alarm rate was slightly higher, ranging from 5 to 25%

(mean = 13.8 ± 6.1%).

Discussion

This study is the first to describe a CSF in a marine

mammal, the harbor seal. Herein, we report the results

from one individual that was available for this time-con-

suming experiment. To determine whether the obtained

data are representative for the species, data from other

individuals would be needed. However, the experimental

animal tested for contrast sensitivity has taken part in

numerous psychophysical experiments, including vision

(Hanke FD et al. 2006; Hanke W et al. 2006; Weiffen et al.

2006; Hanke et al. 2008b; Hanke and Dehnhardt 2009), and

does not show any visual deficits during daily tasks. It

performed reliably during contrast sensitivity testing, and

there is close agreement between the results of the study at

hand and of the visual acuity experiments (Hanke and

Dehnhardt 2009) which make our data concerning this

individual reliable.

The shape of the seal’s CSF compares well with the CSF

of other species such as goldfish (Carassius auratus;

Northmore and Dvorak 1979; Bilotta and Powers 1991),

eagle (Aquila audax; Reymond and Wolfe 1981), pigeon

(Columba livia; Nye 1968; Hodos et al. 2003), barn owl

(Tyto alba pratincola; Harmening et al. 2009), tree shrew

(Tupaia belangeri; Petry et al. 1984), rabbit (Pak 1984),

hooded and albino rats (Rattus norvegicus; Birch and

Jacobs 1979; Legg 1984), domestic cat (Felis domesticus;

Campbell et al. 1973; Bisti and Maffei 1974; Blake et al.

1974; Pasternak and Merigan 1981; Blake 1982; Kang

et al. 2009), owl monkey (Aotus trivirgatus; Jacobs 1977),

squirrel monkey (Saimiri sciureus; Merigan 1976), and

macaque (Macaca nemestrina and Macaca fascicularis; De

Valois et al. 1974). Figure 4 shows a direct comparison of

the seal’s CSF with the CSF of goldfish (Northmore and

Dvorak 1979; Bilotta and Powers 1991), cat (Bisti and

Maffei 1974; Blake et al. 1974; Pasternak and Merigan

1981), and human (Bisti and Maffei 1974). The seal’s CSF

can be characterized by the function published by Uhlrich

et al. (1981). It peaks at an intermediate spatial frequency,

and sensitivity decreases to both ends of the spatial fre-

quency range. We observe the characteristic low frequency

roll-off and the high frequency cut-off towards the seal’s

maximal resolution. The cut-off determined by fitting the

contrast sensitivity data compares favorably with the visual

acuity values obtained previously (Hanke and Dehnhardt

2009), which are indicated in Fig. 3 with arrows at the

x axis for adaptation lights comparable to the light used in

this study. As observed in other species, the cut-off fre-

quency is localized approximately 3 octaves from the

maximum of the CSF, and the width at half amplitude of

approximately 3.2 octaves is well within the published

range (Uhlrich et al. 1981).

In contrast to the similarity in shape and width at half

amplitude, the location of the peak spatial frequency and

the absolute peak contrast sensitivity was generally found

to be highly variable across species (Uhlrich et al. 1981)

(cf. Fig. 4). The diverse visual systems seem to behave as if

they possess a similar bandpass spatial filter whose peak

frequency is located at different points in the spatial fre-

quency spectrum. The variation of the location of the peak

1

10

100

1000

spatial frequency (cycles/deg)

cont

rast

sen

sitiv

ity

a b

c

d e

f

g

h

1000.01 0.1 1 10

Fig. 4 Comparison of the contrast sensitivity function (CSF) of the

harbor seal (open circles) to the CSF of a–c goldfish (dotted lines), d–

g cat (solid lines), h human (dashed line). References and mean

luminance of the display for the respective curves: a, b Bilotta and

Powers (1991), a 0.001 cd/m2, b 10 cd/m2, c Northmore and Dvorak

(1979), 23 cd/m2, d, e Pasternak and Merigan (1981), d 0.16 cd/m2,

e 16 cd/m2, f Bisti and Maffei (1974), 2 cd/m2, g Blake et al. (1974),

17.1 cd/m2, h Bisti and Maffei (1974), 2 cd/m2. Of each study, the

curve with the highest contrast sensitivity determined at a mean

luminance of the display close to the mean luminance used in the

study on harbor seal contrast sensitivity (ambient luminance 0.9 lx/

0.5 cd/m2, mean luminance of display 3.8 cd/m2) was chosen for

comparison. Conventions as in Fig. 3a

J Comp Physiol A (2011) 197:203–210 207

123

of the CSF and the absolute values might mirror inter-

specific differences related to the species’ niche and life

style. Alternatively, part of the observed variation might be

related to the diverse methodologies used to assess contrast

thresholds, different definitions of thresholds across the

various studies, or variation in subject motivation and

experimental experience.

An aspect that complicates cross-species comparison

and is critical for harbor seals due to their light sensitive

eyes is that the adaptation light under which contrast

sensitivity was tested is not consistent among studies (cf.

Fig. 4). It was shown in macaque, cat, eagle, and human

that decreasing ambient light causes the location of the

peak of the CSF to shift to a slightly lower frequency,

and the height of the peak to a drastically lower value

(De Valois et al. 1974; Pasternak and Merigan 1981;

Reymond and Wolfe 1981; Bilotta and Powers 1991;

Kang et al. 2009). However, contrast sensitivity changes

to different degrees depending on the respective species.

Comparison of contrast sensitivity in cats and humans

(Pasternak and Merigan 1981; Kang et al. 2009) dem-

onstrated that the change with decreasing ambient light

is more pronounced in humans than in cats leading to

almost equal performance of both species in dim light,

whereas in bright light, human contrast sensitivity

exceeds the cat’s by far.

We tested our harbor seal in weak ambient light

(0.5 cd/m2, mean luminance of display 3.8 cd/m2), which

we chose because low illumination is expected to char-

acterize the visual environment of harbor seals most of

the time. Second, this illumination provides the possi-

bility for comparison with the previously published data

(Scholtyssek et al. 2008; Hanke and Dehnhardt 2009).

Under the experimental conditions set in this study, the

seal’s contrast sensitivity peak lies at approximately

0.5 cycles/deg with an absolute peak height of approxi-

mately 40. The position of the peak at a rather low

frequency points to the fact that harbor seals seem to

make use of their visual system at close viewing dis-

tances which was already outlined by Scholtyssek et al.

(2008). The position and height of the peak of the seal’s

CSF are in good agreement with the data obtained under

comparable experimental conditions in cats (Bisti and

Maffei 1974; Blake et al. 1974; Pasternak and Merigan

1981) (Fig. 4). The seal’s CSF conforms best to the data

presented by Pasternak and Merigan (1981) in terms of

absolute sensitivity and peak position (Fig. 4, curve d).

This general correspondence can probably be explained

by similarities in lifestyle, the visual environment and

the resulting adaptations of the visual system. The eyes

of both species balance resolution and sensitivity; this

equilibrium is needed because they are carnivores often

hunting in dim light. An aquatic species that shares a

visual system equipped for low light levels is the gold-

fish (Northmore and Dvorak 1979; Bilotta and Powers

1991). The contrast sensitivity peak of goldfish is also

found at a location close to the seal’s and cat’s, and the

goldfish’s absolute sensitivity assessed at comparable

ambient luminance (Bilotta and Powers 1991) (Fig. 4,

curve a) is in the same range as the absolute sensitivity

of the other species. Thus, the goldfish’s different feed-

ing ecology and food acquisition does not seem to lead

to general differences in contrast sensitivity.

Harbor seals face the challenges of an amphibious

lifestyle. There is experimental evidence that harbor seals

are emmetropic under water mediated by a spherical lens

and can achieve an aerial visual acuity comparable to the

underwater visual acuity by a static interaction between a

corneal astigmatism and the slit-shaped pupil in bright light

conditions (Hanke FD et al. 2006; Hanke and Dehnhardt

2009). However, with decreasing ambient light and thus

pupils that dilate wider than the corneal flattening aerial

visual acuity decreases which might be due to deflected

light from the stronger curved peripheral cornea and due to

summation. Owing to these observations and the large

changes in contrast sensitivity observed in other species, it

would be interesting to test harbor seal’s contrast sensitivity

under a broad range of adaptation light in a future experi-

ment to assess how the seal’s visual performance varies

within this parameter. We would expect only slight changes

in the position of the peak of the CSF, but large changes in

the height of the CSF, which might be more pronounced in

air than under water due to corneal effects (Hanke and

Dehnhardt 2009). The results of the visual acuity experi-

ments (Schusterman and Balliet 1970; Weiffen et al. 2006;

Hanke and Dehnhardt 2009) imply that the cut-off fre-

quency can shift to at least 5.5 cycles/deg in bright light and

clear waters. Furthermore, it remains to be investigated if

the joint effect of corneal astigmatism, favoring resolution

of vertical stimuli, and the pinhole effect of the pupil,

favoring resolution of horizontal stimuli, results in different

contrast sensitivity for vertical and horizontal stimuli in air.

Under water, a different importance of the horizontal and

vertical plane, which could also affect the resolution in the

respective meridians, has already been questioned in seals

(Hanke et al. 2008a, 2009b) and sea lions (Mauck and

Dehnhardt 1997; Stich et al. 2000), as their environment is

three-dimensional and head and body can rotate in all

directions. In cats contrast sensitivity measurements in

various meridians did not reveal any systematic difference

between the meridians (Campbell et al. 1973; Bisti and

Maffei 1974). In humans, a slightly reduced contrast sen-

sitivity for oblique orientations was found (Campbell et al.

1966; Maffei and Campbell 1970).

To conclude, the seal’s CSF shows the general charac-

teristics of CSFs obtained in other vertebrate species. Its

208 J Comp Physiol A (2011) 197:203–210

123

parameters are specifically in close agreement with the

CSF of cats, a species that, except for the amphibious

lifestyle of seals, shares the carnivorous lifestyle and

optical adaptations for dim light vision.

Acknowledgments The authors would like to acknowledge the

valuable help of Viljami Salmela (Helsinki, Finland). Thanks is also

expressed to Sophie Fiedler for assistance during data collection and

to Christopher D. Marshall (Galveston, TX, USA) for critically

reading the manuscript. This study was financially supported by a

grant of the Studienstiftung des deutschen Volkes (2005 SA 0969) to

FDH and of the Deutsche Forschungsgemeinschaft (SFB 509, DE

538/10-1) as well as the Volkswagenstiftung to GD. The experiments

are in line with the current German law on the protection of animals.

References

Bilotta J, Powers MK (1991) Spatial contrast sensitivity of goldfish:

mean luminance, temporal frequency and a new psychophysical

technique. Vis Res 31(3):577–585

Birch D, Jacobs GH (1979) Spatial contrast sensitivity in albino and

pigmented rats. Vis Res 19:933–937

Bisti S, Maffei L (1974) Behavioural contrast sensitivity of the cat in

various visual meridians. J Physiol 241:201–210

Blake R (1982) Binocular vision in normal and stereoblind subjects.

Am J Optom Physiol Opt 59(12):969–975

Blake R, Cool SJ, Crawford MLJ (1974) Visual resolution in the cat.

Vis Res 14:1211–1217

Campbell FW, Kulikowski JJ, Levinson J (1966) The effect of

orientation on the visual resolution of gratings. J Physiol

187:427–436

Campbell FW, Maffei L, Piccolino M (1973) The contrast sensitivity

of the cat. J Physiol 229:719–731

Cronin TW (2006) Invertebrate vision in water. In: Warrant EJ,

Nilsson D-E (eds) Invertebrate vision. University Press, Cam-

bridge, pp 211–249

Davis RW, Wartzok D, Elsner R, Stone H (1992) A small video

camera attached to a Weddell seal: a new way to observe diving

behavior. In: Thomas J et al (eds) Marine mammal sensory

systems. Plenum, New York, pp 631–642

Davis RW, Fuiman LA, Williams TM, Collier SO, Hagey WP,

Kanatous SB, Kohin S, Horning M (1999) Hunting behaviour of

a marine mammal beneath the Antarctic fast ice. Science

283:993–996

De Valois RL, Morgan H, Snodderly DM (1974) Psychophysical

studies of monkey vision—III. Spatial luminance contrast

sensitivity tests of macaque and human observers. Vis Res

14:75–81

Duntley SQ (1963) Light in the sea. J Opt Soc Am 53:214–233

Gellermann LW (1933) Chance orders of alternating stimuli in visual

discrimination experiments. J Gen Psychol 42:206–208

Ginsburg AP, Evans DW, Sekule R, Harp SA (1982) Contrast

sensitivity predicts pilots’ performance in aircraft simulators.

Am J Optom Physiol Opt 59(1):105–109

Hanke FD, Dehnhardt G (2009) Aerial visual acuity in harbor seals

(Phoca vitulina) as a function of luminance. J Comp Physiol A

195:643–650

Hanke FD, Dehnhardt G, Schaeffel F, Hanke W (2006) Corneal

topography, refractive state, and accommodation in harbor seals

(Phoca vitulina). Vis Res 46:837–847

Hanke FD, Hanke W, Hoffman K-P, Dehnhardt G (2008a) Optoki-

netic nystagmus in harbor seals (Phoca vitulina). Vis Res

48(2):304–315

Hanke FD, Kroger RHH, Siebert U, Dehnhardt G (2008b) Multifocal

lenses in a monochromat: the harbour seal. J Exp Biol

211:3315–3322

Hanke FD, Hanke W, Scholtyssek C, Dehnhardt G (2009a) Basic

mechanisms in pinniped vision. Exp Brain Res 199(3):299–311

Hanke FD, Peichl L, Dehnhardt G (2009b) Retinal ganglion cell

topography in juvenile harbor seals (Phoca vitulina). Brain

Behav Evol 74:102–109

Hanke W, Romer R, Dehnhardt G (2006) Visual fields and eye

movements in a harbor seal (Phoca vitulina). Vis Res

46:2804–2814

Harmening WM, Nikolay P, Orlowski J, Wagner H (2009) Spatial

contrast sensitivity and grating acuity of barn owls. J Vis

9(7):1–12

Hobson ES (1966) Visual orientation and feeding in seals and sea

lions. Nature 210:326–327

Hodos W, Potocki A, Ghim MM, Gaffney M (2003) Temporal

modulation of spatial contrast vision in pigeons (Columba livia).

Vis Res 43:761–767

Jacobs GH (1977) Visual capacities of the owl monkey (Aotustrivirgatus)—II. Spatial contrast sensitivity. Vis Res 17:821–825

Jamieson GS, Fisher HD (1972) The pinniped eye: a review. In:

Harrison RJ (ed) Functional anatomy of marine mammals.

Academic Press, London, pp 245–261

Kang I, Reem RE, Kaczmarowski AL, Malpeli JG (2009) Contrast

sensitivity of cats and humans in scotopic and mesopic

conditions. J Neurophysiol 102(2):831–840

Kroger RHH (2008) The physics of light in air and water. In:

Thewissen JGM, Nummela S (eds) Sensory evolution on the

threshold—adaptations in secondarily aquatic vertebrates. Uni-

versity of California Press, Berkeley, pp 113–119

Kroger RHH, Katzir G (2008) Comparative anatomy and physiology

of vision in aquatic tetrapods. In: Thewissen JGM, Nummela S

(eds) Sensory evolution on the threshold—adaptations in

secondarily aquatic vertebrates. University of California Press,

Berkeley, pp 121–147

Legg CR (1984) Contrast sensitivity at low spatial frequencies in the

hooded rat. Vis Res 24(2):159–161

Maffei L, Campbell FW (1970) Neurophysiological localization of

the vertical and horizontal visual coordinates in man. Science

167:386–387

Mauck B, Dehnhardt G (1997) Mental rotation in a California sea lion

(Zalophus californianus). J Exp Biol 200:1309–1316

Merigan WH (1976) The contrast sensitivity of the squirrel monkey

(Saimiri sciureus). Vis Res 16:375–379

Nordmann JP, Freeman RD, Casanova C (1992) Contrast sensitivity

in amblyopia: masking effects of noise. Invest Ophthalmol Vis

Sci 33(10):2975–2985

Northmore DPM, Dvorak CA (1979) Contrast sensitivity and acuity

of the goldfish. Vis Res 19:255–261

Nye PW (1968) The binocular acuity of the pigeon measured in terms

of the modulation transfer function. Vis Res 8:1041–1053

Olzak LA, Thomas JP (1986) Seeing spatial patterns. In: Boff K,

Kaufman L, Thomas JP (eds) Handbook of perception and

human performance. Wiley, New York, pp 7.1–7.56

Owsley C, Sloane ME (1987) Contrast sensitivity, acuity, and the

perception of ‘real-world’ targets. Br J Ophthalmol 71:791–796

Pak MA (1984) Ocular refraction and visual contrast sensitivity of the

rabbit, determined by the VECP. Vis Res 24(4):341–345

Pasternak T, Merigan WH (1981) The luminance dependence of

spatial vision in the cat. Vis Res 21:1333–1339

Petry HM, Fox R, Casagrande VA (1984) Spatial contrast sensitivity

of the tree shrew. Vis Res 24(9):1037–1042

Reuter T, Peichl L (2008) Structure and function of the retina in

aquatic tetrapods. In: Thewissen JGM, Nummela S (eds) Sensory

evolution on the threshold—adaptations in secondarily aquatic

J Comp Physiol A (2011) 197:203–210 209

123

vertebrates. University of California Press, Berkeley,

pp 149–172

Reymond L, Wolfe J (1981) Behavioural determination of the

contrast sensitivity function of the eagle Aquila audax. Vis Res

21:263–271

Scholtyssek C, Kelber A, Dehnhardt G (2008) Brightness discrimi-

nation in the harbor seal (Phoca vitulina). Vis Res 48:96–103

Schusterman RJ, Balliet RF (1970) Visual acuity of the harbour seal

and the Steller sea lion under water. Nature 226:563–564

Stich KP, Dehnhardt G, Mauck B (2000) Mental rotation of

perspective stimuli in a California sea lion (Zalophus californi-anus). Brain Behav Evol 61:102–112

Uhlrich DJ, Essock EA, Lehmkuhle S (1981) Cross-species corre-

spondence of spatial contrast sensitivity functions. Behav Brain

Res 2:291–299

Warrant EJ, Locket NA (2004) Vision in the deep sea. Biol Rev

79:671–712

Weiffen M, Moller B, Mauck B, Dehnhardt G (2006) Effect of water

turbidity on the visual acuity of harbor seals (Phoca vitulina).

Vis Res 46:1777–1783

Woods RL, Wood JM (1995) The role of contrast sensitivity charts

and contrast letter charts in clinical practice. Clin Exp Ophthal-

mol 78(2):43–51

210 J Comp Physiol A (2011) 197:203–210

123