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First published online October 7, 2008
Journal of Experimental Biology 211, 3315-3322 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.018747
Multifocal lenses in a monochromat: the harbour seal
1 University of Bochum, General Zoology and Neurobiology, ND 6/33, D-44780
Bochum, Germany
2 Lund University, Department of Cell and Organism Biology, Zoology Building,
Helgonavägen 3, S-22362 Lund, Sweden
3 University of Kiel, Research and Technology Centre West Coast,
Werftstraße 6, D-21542 Büsum, Germany
4 University of Rostock, Institute for Bioscience, Sensory and Cognitive
Ecology, Albert-Einstein-Strasse 3, D-18059 Rostock, Germany
* Author for correspondence (e-mail: dehnhardt{at}marine-science-center.de)
Accepted 18 August 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: harbour seal, Phoca vitulina, lens, multifocal
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Marine mammals are secondarily adapted to the aquatic environment. The
spherical state of their crystalline lenses compensates to some extent for the
loss of corneal refractive power under water
(Jamieson and Fisher, 1972
).
So far, little is known about lens optics in marine mammals in general and in
pinnipeds in particular. In whales, measurements revealed that the harbour
porpoise (Phocoena phocoena) lens brings parallel light to a focus in
front of the retina (Matthiessen,
1886; Matthiessen,
1893; Kröger,
1989; Kröger and
Kirschfeld, 1992; Kröger
and Kirschfeld, 1993). In these eyes, the cornea acts as a
diverging lens under water. To our knowledge, the only study examining lens
optics in a pinniped species, the hooded seal (Cystophora cristata),
was conducted by Sivak et al. (Sivak et
al., 1989). The authors reported that hooded seal lenses are
spherical in shape and have short focal lengths. According to the results of
that study, the lenses are well corrected for spherical aberration.
While performing photorefractive measurements on harbour seal eyes
(Hanke et al., 2006), we
observed ring-shaped brightness distributions under water, reminiscent of the
brightness distributions indicative of multifocal lenses
(Kröger et al., 1999;
Malkki and Kröger, 2005).
The evolution of such lenses served to compensate for the chromatic defocus
that occurs because the refractive index of any transparent material increases
with decreasing wavelength. Consequently, the focal length of a lens is a
function of the wavelength of light (longitudinal chromatic aberration, LCA).
This implies that at any time, only a narrow band of wavelengths can be in
focus on the retina in the absence of a compensatory mechanism. Light of other
wavelengths is defocused (chromatic defocus). Chromatic defocus is especially
unwanted in species capable of colour vision and with eyes with a short depth
of focus. The evolution of multifocal lenses has solved the problem of
chromatic defocus as these lenses create well-focused images at the
wavelengths of maximum absorbance (
max) of the cone
photoreceptors (Kröger et al.,
1999). First described for a cichlid fish
(Kröger et al., 1999),
multifocal lenses seem to be widespread among vertebrates
(Malkki and Kröger, 2005;
Malmström and Kröger,
2006; Karpestam et al.,
2007; Gustafsson et al.,
2008; Lind et al.,
2008).
The ring-shaped brightness distributions in photorefractive images as a
first indication of multifocal lenses in harbour seals were unexpected as
harbour seals are said to be colour-blind because of the absence of the
short-wave-sensitive cone type (Peichl and
Moutairou, 1998; Crognale et
al., 1998; Peichl et al.,
2001; Newman and Robinson,
2005; Levenson et al.,
2006); however, this still leaves the possibility of mesopic
colour vision, which is currently under investigation in our lab. Furthermore,
the ring-shaped brightness distributions in seal pupils were atypical because
they could only be observed under water and only along the optical axis. These
contradictory findings, together with the fact that no detailed information on
pinniped lenses is available, led us to examine lens optics in juvenile
harbour seals with modern optical techniques as described by Malkki and
Kröger (Malkki and Kröger,
2005). In addition, we repeated and extended our photorefractive
measurements under water and in air in two live, adult seals.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Photorefractive measurements
Photorefractive measurements under water and in air were performed using
IR-photoretinoscopy as developed by Schaeffel et al.
(Schaeffel et al., 1987) and
described in detail by Hanke et al. (Hanke
et al., 2006). The IR-photoretinoscope
(Fig. 1A, inset) consisted of a
metal shield that covered one half of the lens aperture (lens:
Cosmicar/Pentax, F=50 mm, f/1:1.4, Hamburg, Germany; with two
extension rings, resulting in an operating distance of 0.5 m) of an
IR-sensitive monochrome CCD camera (The Imaging Source, Bremen, Germany). The
light of 13 IR-LEDs (light emitting diodes) on the IR-retinoscope,
eccentrically arranged in four horizontal rows, entered the eye, was reflected
and produced a brightness distribution in the pupil. Photorefractive
measurements under water and in air were performed in darkness in order to
dilate the pupils. The camera and retinoscope were placed at a distance of 0.5
m in front of the eye with the knife edge of the retinoscope (edge of the
metal shield in the lens aperture) (Fig.
1A, inset) orientated horizontally. For underwater measurements,
the animal climbed onto a small platform and immersed its head in a
water-filled aquarium made of glass (Fig.
2). After lowering the head, the eyes were close to the aquarium's
front window.
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Preparation of the lenses
To facilitate the removal of the eye out of the orbit, large parts of the
eyelids were removed. The eye muscles were detached from the eyeball and the
optic nerves were cut. Due to the thickness of the lens and its close
adherence to the vitreous (Fig.
3B), the eye was opened anteriorly via the corneal
periphery. First, the cornea and iris were completely removed. Second, the
lens was excised by cutting the zonular fibres almost all around the lens.
Some zonular fibres with their associated ciliary body and neighbouring sclera
(approximately 5 mmx5 mm) (Fig.
3A) were left attached. This served as a handle, which allowed the
lens to be placed in the setups with minimal manipulation. During dissection,
the vitreous was found to be strongly adherent to the posterior surface of the
lens (Fig. 3B), as is
encountered in the young human eye
(Sachsenweger, 2003). Although
in each case an attempt was made to remove this vitreous carefully from the
lens, without damage, it was not always certain that removal was complete,
except in seal 4.
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The lens of the first eye was extracted between 0.5 and 2.5 h after the death of the animal (Table 1). The second eye was excised approximately one hour later, after the measurements on the first lens had been completed.
Schlieren photography
The portable setup described by Malkki and Kröger
(Malkki and Kröger, 2005)
was used in this study. In schlieren photography, white light from a point
source (standard cold light laboratory lamp running at 3200 K) was reflected
by a beam splitter into the optical axis
(Fig. 1B). The seal lens was
suspended in an immersion bath filled with phosphate buffered saline (PBS,
pH=7.4, 290 mosmol, approximately 20°C) and focused the light beam on a
diffuse reflector at the rear side of the immersion bath. Reflected light was
focused by the lens on the pinhole and was recorded by a digital video camera
(Sony DCR-TRV620E PAL, Sony Corporation, Tokyo, Japan). Different from Malkki
and Kröger (Malkki and Kröger,
2005), it was not necessary to further magnify the picture.
Each freshly excised lens was inserted directly into the schlieren setup with the posterior pole of the lens facing the diffuse reflector. The posterior pole was identified from the lens's orientation in the eye-cup. Care was taken to keep the lens orientated correctly throughout all experiments.
Laser scanning
Laser scan setup
The video camera used in schlieren photography was transferred to the
portable laser scan setup (Malkki and
Kröger, 2005), video recording the immersion bath at a
distance of 10 cm from above (Fig.
1C). The image's long axis was slightly turned (approximately 10
deg.) relative to the laser beam in order to minimize aliasing effects. The
immersion bath contained PBS (pH=7.4, 290 mosmol, approximately 20°C) to
which one drop of microparticles had been added to scatter light and,
therefore, gain a high visibility of the laser beam. The seal lens was then
positioned on a holder in the middle of the immersion bath with the help of
the forceps used in schlieren photography. The posterior pole of the lens was
facing the rear side of the immersion bath. The position of the lens was
further modified by manually rotating the lens and/or the lens holder with
respect to the laser beam until the optical axis of the lens was aligned with
the laser beam. This could be achieved by adjusting the zonular fibre ring to
be perpendicular to the laser beam when viewing the immersion bath from the
top and from the side. The remaining piece of sclera was removed immediately
after positioning of the lens. The large size of the seal's lens obviated the
need for magnification used for measuring fish lenses
(Malkki and Kröger,
2005). A 5 mW green (537 nm) diode-pumped, solid-state laser was
used to scan the lens. The laser beam was focused with an F=100 mm lens with
the meniscus of the focused laser beam placed directly in front of the seal
lens that re-collimated the beam. The laser beam was then adjusted in height
until it passed through the centre of the seal lens without being deflected.
The translation stage on which the laser and its focusing unit were mounted
could only be moved to scan two thirds of the large seal lenses. Therefore,
the same lens was scanned twice, once starting from the left side and once
from the right side, while the camera was video recording the light of the
laser beam, which was scattered upwards by the microparticles. Laser scanning
experiments were performed with only one wavelength because the obtained
results are largely independent of the wavelength, except for a longitudinal
shift, within the visible range of the spectrum
(Kröger and Campbell,
1996).
Analysis of laser scans
From each scan, 200 frames were exported in TIFF (tagged image file
format). We used a custom-written program (in IDL 6.0 developing environment,
Research Systems, Boulder, CO, USA), which has been described in detail by
Malkki and Kröger (Malkki and
Kröger, 2005), for analysis of the back centre distance (BCD,
axial distance between the lens centre and the intercept between the exit beam
and the optical axis of the lens) as a function of beam entrance position
(BEP, lateral distance between the entrance beam and the optical axis). This
function describes the longitudinal spherical aberration (LSA) of the lens.
The two scans per lens (see above) were analyzed separately. After acquiring
laser beam data at each laser position by the program, an image was generated
by averaging all exported frames. On this image, the axial and equatorial
diameters of the lens were determined manually. As we always had laser scans
extending over only approximately two thirds of the equatorial diameter of the
lens, we had to estimate the equatorial diameter. However, there were always
enough data points from the second half of the lens to adjust the optical axis
of the lens in the last step of analysis
(Malkki and Kröger,
2005). In Microsoft Excel (The Microsoft Corporation, Redmond, WA,
USA), the results from both scans through each lens were averaged because
there was very good agreement in the region covered by both scans.
Measurement of refractive index and osmolarity of the aqueous and vitreous humours
Extraction of aqueous and vitreous
Before opening the eye, an injection needle was gently inserted into the
anterior chamber of the eye via the cornea and approximately 1 ml of
aqueous was extracted with a syringe. The syringe and its content were
immediately deep-frozen at –80°C until measurements could be
performed. Some of the vitreous was cut out of the eye-cup after removing the
lens and placed into Eppendorf tubes. These tubes were also stored at
–80°C.
Determination of eye and lens dimensions, refractive index and osmolarity
Equatorial diameter of the eye-cup and both diameters of the lenses were
measured with sliding callipers after the optical measurements had been
performed. The accuracy of the measurements was estimated as 0.1 mm. For the
determination of refractive index and osmolarity of the aqueous and vitreous
humours, the deep-frozen samples were thawed. Refractive index was determined
at 22°C with a digital Abbe refractometer (DR 5000, Krüss Optic,
Hamburg, Germany). Osmolarity was measured with an osmometer (The Advanced
Micro Osmometer Model 3300, Advanced Instruments, Norwood, MA, USA).
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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),
ring-shaped brightness distributions are apparent on photorefractive pictures
obtained under water (Fig.
4A–C). However, extended measurements revealed that these
rings are always visible, even if recordings were off-axis and the eye was
slightly ametropic. One very prominent ring appears in the periphery of the
lens but only when the pupil is fully dilated
(Fig. 4A–C). Two faint
rings are present at approximately 0.5 lens radius (R) and 0.75 R
(Fig. 4A). All rings are more
pronounced in the adult seal (Fig.
4C). In air, somewhat masked by reflections from the corneal
surface (Hanke et al., 2006)
and by corneal distortions, rings are not as prominent but can still be
detected between approximately 0.65 and 0.75 R
(Fig. 4D).
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Due to the complete removal of the vitreous humour from the lenses of seal 4 (Fig. 5D), the respective schlieren photographs are most reliable. There are two broad bluish rings, one thin dark-blue ring and a red outer ring. These features are in keeping with the results of photorefractive measurements in the young seal under water (Fig. 4A) with the two bluish rings correlating to the two more central rings and the thin dark-blue ring corresponding to the prominent ring at approximately 0.85 R. The lens sutures are prominent on all schlieren photographs (Fig. 5). They stretch over almost 0.8 R and are of cross-like appearance.
Laser scans
The results are irregular for the central BCDs between 0 and 0.3 R
(Fig. 6A–D) where the
accuracy of the method is low (Malkki and
Kröger, 2005). The obtained LSA curves vary between
individuals. However, as a common feature, all LSA curves, except for the
scans of the newborn (Fig. 6A),
show two peaks in the periphery (Fig.
6B–D, long arrows). Furthermore, a sharp decline in BCD
towards the outermost periphery is evident in all analyzed lenses
(Fig. 6A–D, short
arrows). The mean LSA curve of all, except for the lenses of the neonate, is
presented in Fig. 7A. Two peaks
of slightly different BCDs can be seen (first peak at BEP 0.67 R, BCD 3.77 R;
second peak at BEP 0.87 R, BCD 3.75 R). The mean BCD between 0.3 and 0.6 R is
3.58 R. BCD increases minimally towards the centre by 0.05 R (1.4% of mean
value 3.58 R). At 0.9 R, BCD drops steeply by approximately 0.5 R (14% of mean
value 3.58 R) before increasing again up to values of approximately 5R. The
mean LSA curve (Fig. 7A)
mirrors the results of photorefractive measurements in the live seals under
water (Fig. 4A–C) and the
schlieren photographs of the best dissected lens
(Fig. 5D) as again two broad
rings and a thin sharp ring can be discerned clearly.
Fig. 7B shows the averaged
picture of one laser scan presenting all laser beams entering the lens and the
way they are deflected by the lens.
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Eye and lens dimensions, refractive index and osmolarity of the aqueous and vitreous humours
All eye and lens dimensions as well as refractive index and osmolarity
measurements are listed in Table
2. Due to the dissection process and the need for minimizing the
time between the animal's death and the start of the experiments, only the
equatorial diameter of the eye-cup could be measured with a mean
(±s.d.) value of 33.0±0.08 mm
(Table 2). The equatorial
diameter of the eye-cup was slightly larger in older animals
(Table 2).
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The lenses were clear and almost spherical in shape. In all lenses, the equatorial diameter is slightly larger than the axial diameter. Mean axial lens diameter (±s.d.) is 10.90±0.19 mm, mean equatorial diameter (±s.d.) 11.69±0.33 mm (Table 2).
The aqueous and vitreous humours both have approximately the same mean refractive index of 1.335 (aqueous, 1.33498±0.00032, N=7; vitreous, 1.33454±0.00010, N=6; Table 2). Mean osmolarity of both media is 343.6 mosmol (aqueous, 344.571±22.397 mosmol, N=7; vitreous, 342.667±12.127 mosmol, N=6; Table 2).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Malmström and Kröger,
2006; Karpestam et al.,
2007; Gustafsson et al.,
2008; Lind et al.,
2008). Although methodological limitations have to be considered
(see Methodological limitations, below), we assume the distinctive refractive
zones to be of functional significance for vision in harbour seals (see
Optical status of harbour seal lenses, below).
Methodological limitations
Photorefractive measurements in live animals
We ascribe the main role in the generation of the rings in photorefractive
images to the lens because of the similarity of the rings obtained by all
methods applied. Scattering of light inside the lens is an unlikely cause for
the occurrence of the rings because scattering would make them appear dark.
Corneal shape and irregularities have an effect on the brightness profiles in
air (Fig. 4D)
(Hanke et al., 2006) but their
effect on underwater photorefraction is expected to be negligible.
The nature of the sharp ring in the periphery seen only in fully dilated pupils remains speculative. To clarify whether it mirrors a functional feature in the optically relevant part of the lens or reflects the lens's very periphery that is normally shaded by the iris, more data from the lens periphery are needed.
Optical quality of extracted lenses
All lenses studied were extracted from very young seals with potentially
immature lenses. If they were indeed immature, which means not fully
developed, the results of this study might not be representative for the
optical status of the adult seal's eye. The variation in the results might
suggest that the lenses were still under developmental fine-tuning. However,
due to the short mother–pup relation in phocid seals
(Bowen, 1992;
Atkinson, 1997) there might be
a strong selection pressure on developing fully mature sensory organs shortly
after birth enabling the juvenile animals to hunt and navigate independently.
The juvenile lenses we studied were therefore most likely already optically
similar to adult lenses.
The lenses were free of cataracts that could have been induced by the
overall weakness or illness of the seals (see Lens measurements, above),
nutritional deficiencies due to raising on milk replacer
(Bunce, 1979), or as
post-mortem changes. Furthermore, the lenses may have absorbed some water in
the periphery because it turned out that the osmolarity in seal eyes is
approximately 53 mosmol higher compared with the PBS used in the present
study, which was iso-osmotic to the body fluids of humans and other
terrestrial mammals. However, the difference in osmolarity is overestimated to
some extent, as some water has probably evaporated from the frozen samples of
aqueous and vitreous humours.
Schlieren photography and laser scanning
Some vitreous humour remained attached to the posterior sides of the lenses
(see Preparation of the lenses, above). However, as the vitreous has a
refractive index similar to the solution in the immersion baths, its influence
was probably minor.
On schlieren photographs of the lenses of seal 1, being the youngest, the coloured part is smaller than the lens itself. The laser scanning results show that the dark part has a considerably shorter focal length than other regions of the lens (Fig. 6A), which suggests that it focused IR-wavelengths on the pinhole in the schlieren setup. This in turn suggests that the periphery of very young seal lenses does not contribute to vision.
Because of their apparent immaturity, we excluded the lenses of seal 1 from
the analysis of the laser scanning data. The remaining results from laser
scanning are still variable, probably reflecting some residual immaturity.
Another source of error is the low accuracy of the laser scanning method for
BEPs smaller than 0.3R (Malkki and
Kröger, 2005). However, this central region of a lens covers
a small area and has long depth of focus, such that it contributes little to
retinal illumination and blur. Damage to the lens, inflicted during excision,
and the lens sutures are other sources of variability
(Kuszak et al., 1991;
Sivak et al., 1994) since only
one meridian is probed by laser scanning. Results from individual scans are
therefore rarely reliable. The LSA curve obtained by averaging all scanning
results (Fig. 7A) is more
trustworthy and will be discussed further (see Optical status of harbour seal
lenses, below), although variation intrinsic to the individual lens will be
hidden. The results of laser scanning that are generally susceptible to noise
are consistent with the results from the two other methods applied, which
leads us to conclude that the complex LSA observed in the mean LSA curve
represents not just regular spherical aberration, which is typical for a
spherical lens but serves to compensate for LCA.
Optical status of harbour seal lenses
There are visible rings on photorefractive pictures obtained from adult
seals (Fig. 4). Furthermore,
there are two peaks in the mean LSA curves at approximately 0.67R and 0.87R
(Fig. 7A). These peaks
correspond well to bluish rings on schlieren photographs
(Fig. 5), the outer one of
these being narrow in the lenses of seal 3
(Fig. 5C). In total, our
results from three different methods strongly suggest that harbour seals have
multifocal lenses. Even if the refractive zones of seal lenses are not as well
defined as in many fish lenses
(Kröger et al., 1999;
Karpestam et al., 2007), the
optical principle seems to be the same, i.e. compensation for LCA by complexly
shaped LSA. The method of focal-area imaging, which we did not apply because
up to now no portable setup is available
(Malkki and Kröger,
2005), could clarify whether seal lenses are indeed able to
concentrate different wavelengths of light on small focal areas by directly
analyzing the shape of the cone of light exiting the lens.
Multifocal optical systems are present in various vertebrate species that
are active under low light conditions, have thick and almost spherical lenses
with the lens centre close to the centre of curvature of the cornea, and with
eyes with small f-numbers
(Kröger et al., 1999;
Malkki and Kröger, 2005;
Malmström and Kröger,
2006; Karpestam et al.,
2007; Gustafsson et al.,
2008). All of these characteristics are present in harbour seal
eyes as well. A number of diurnal birds also have multifocal lenses despite
not meeting the above mentioned criteria; however, these species are sensitive
to short and very short (ultraviolet) wavelengths. Since LCA increases almost
exponentially at the short-wave end of the spectrum
(Hecht, 2002), birds seem to
need multifocal optical systems to compensate for the strong LCA in the blue
to ultraviolet region of the spectrum
(Lind et al., 2008).
Refractive zones of the lens and pupil dynamics
Animals can only profit from multifocal lenses if the different refractive
zones are not covered by the iris. This problem is solved if the pupil is
insensitive to light, as in many fishes
(Kröger et al., 1999), or
if there are slit-shaped pupils, which are considered to be adaptations to
multifocal lenses (Malmström and
Kröger, 2006) because even if the pupil is constricted to a
narrow slit under high ambient light intensities all refractive zones of a
multifocal lens can be used for imaging. Harbour seal irises exhibit a large
range of pupillary area covering all stages from circular to vertical slits
and a pinhole at maximum constriction
(Levenson and Schusterman,
1997). However, according to our own unpublished measurements in
harbour seals, vertical pupil diameter decreases by approximately a factor of
two if light intensity increases from 0.1 cd m–2 (pupil fully
dilated and almost circular) to 80 cd m–2 (pupil constricted
to a small vertical slit). The two peaks, observed in the laser scans, occur
at a beam entrance position of 0.67R and 0.87R and both contribute to the
image if the pupil is fully dilated (radius 1R). However, at 80 cd
m–2, where the pupil's vertical diameter is reduced by a
factor of two, none of the distinct refractive zones focuses light on the
retina, and the multifocal lens is dysfunctional under these intermediate
light intensities. Harbour seals can thus take advantage of the different
refractive zones of the lens only if the pupil is widely dilated, which means
if ambient light intensity is low.
Functional significance of multifocal lenses in harbour seals
Multifocal lenses are described as a solution to the problem of chromatic
defocus (Kröger et al.,
1999). Animals equipped with several spectral types of cone
photoreceptor in the retina profit from multifocal lenses as each focal length
of the lens is used to create a well-focused image for one of the cone
types.
Harbour seals are incapable of cone-based colour vision because the animals
are L-cone monochromats as far as morphological
(Jamieson and Fisher, 1971),
electroretinographic (Crognale et al.,
1998; Levenson et al.,
2006), genetic (Newman and
Robinson, 2005; Levenson et
al., 2006) and immunocytochemical
(Peichl and Moutairou, 1998;
Peichl et al., 2001) analyses
indicate. Surprisingly, multifocal optical systems are also present in some
other cone monochromats (Malmström
and Kröger, 2006). These authors speculated that undiscovered
different spectral types of rod might explain the presence of multifocal
lenses in cone monochromats.
Harbour seals could obtain some colour information by comparing the outputs
of rods and cones under mesopic light conditions
(Crognale et al., 1998).
Consistent with mesopic colour vision, experiments on colour discrimination
tested in psychophysical experiments in four pinniped species so far [Bering
sea spotted seal, Phoca largha
(Wartzok and McCormick, 1978);
two species of fur seals, Arctocephalus pusillus and
Arctocephalus australis (Busch and
Dücker, 1987); California sea lion, Zalophus
californianus (Griebel and Schmid,
1992)] have revealed some colour vision in the blue–green
range of the spectrum. However, except for the study on colour vision in the
Bering sea spotted seal (Wartzok and
McCormick, 1978), the seals might have used brightness instead of
colour cues if the seals' sensitivity for brightness differences had been
underestimated. This hypothesis is supported by the low brightness
discrimination thresholds assessed in Bering sea spotted seals
(Wartzok and McCormick, 1978)
and in harbour seals (Scholtyssek et al.,
2007). Mesopic colour vision, shown in owl monkeys
(Jacobs et al., 1993) and
human blue-cone monochromats (Reitner et
al., 1991), is currently under investigation in our lab in harbour
seals using the lower border of mesopic colour vision in humans as a reference
luminance because mesopic light conditions are not clearly defined for harbour
seals. If the pupil is wide under lighting conditions that are mesopic for
seals (see Photorefractive measurements in live animals, above), the lens
might be optimized for mesopic colour vision in the blue–green range of
the spectrum where the rods and cones have their max. The
rod's max lies at 495–501 nm
(Lavigne and Ronald, 1975;
Fasick and Robinson, 2000;
Levenson et al., 2006),
whereas the cone's max is assumed to be approximately 550
nm (Newman and Robinson, 2005;
Levenson et al., 2006). The
deviating results from Crognale et al.
(Crognale et al., 1998) for the
cone's max, assessed as 510 nm, might be explained by an
overlap of the weak cone signal, which is expected to be weak due to the
sparse population of cones (Peichl and
Moutairou, 1998), by the rod signal. This overlap would have
shifted the spectral sensitivity peak to 510 nm if measurements were
unintentionally conducted under mesopic conditions. Thus, assuming the
max of harbour seal rods and cones to be 496 nm
(Lavigne and Ronald, 1975) and
550 nm, respectively, the difference in focal length is 1.4% [calculated as in
Kröger and Campbell (Kröger and
Campbell, 1996)], which would make multifocal optical systems
beneficial. Harbour seal lenses therefore solve the problem of chromatic
aberration in dim light. In bright light, where the pupil is almost completely
or fully constricted, depth of focus is increased and there is little
chromatic blur. The difference in focal length would be 0.6% in the case of
the rod and cone max at 496 nm and 510 nm
(Crognale et al., 1998),
respectively. Such a small amount of LCA would probably deny the benefit of
multifocal lenses.
One may wonder how colour vision can be beneficial to harbour seals. Colour
is helpful in the detection and identification of objects if they cannot be
distinguished on the basis of intensity. In environments with fast variations
in light intensity, colour offers a reliable cue because the ratio of the
signals from two receptor types is little affected by changes in illumination
(Maximov, 2000;
Kelber et al., 2003). Harbour
seals indeed experience rapid changes in light intensity by wave-induced
flicker when close to the surface and large variations in brightness while
diving. However, their visual systems are highly sensitive to brightness cues
(Jamieson and Fisher, 1972;
Scholtyssek et al., 2007), and
brightness cues as well as contrast might be sufficient for the tasks the
animals have to perform. Furthermore, the appropriate ambient light intensity
for relying on colour cues concerning the essential number of photons
(Lythgoe and Partridge, 1991)
might be rarely met as harbour seals also forage at night or in dark waters at
great depth. Nevertheless, there may be an unknown advantage of colour vision
because the visual ecology of seals is largely unknown.
In addition to a possible function for colour vision, a multifocal lens can
be used to increase depth of focus that is short in seal eyes with small
f-numbers when the pupils are dilated. It may be advantageous if
objects at various distances are simultaneously well-focused without a need
for extensive accommodative abilities
(Hanke et al., 2006). However,
increased depth of focus comes at the cost of reduced contrast because the
in-focus image created by the multifocal lens is overlaid by light from its
out-of-focus images. The highest possible acuity and contrast for small
objects would be obtained with an eye focused on the point of interest using a
monofocal lens. According to the presented data, harbour seals view the world
through a status close to monofocal if the pupil is constricted to such an
extent that light is focused on the retina by just the central parts of the
lens and cornea (see Refractive zones of the lens and pupil dynamics,
above).
Conclusions
Harbour seals seem to possess multifocal lenses as are present in many
other vertebrates. Interestingly, the seal's slit pupil cannot be considered
an adaptation to a multifocal lens. Rather pupil constriction changes the
function of the lens from multifocal in dim light to a status close to
monofocal in bright light. Multiple focal lengths could be beneficial to seals
using mesopic colour vision and by increasing depth of focus in dim light when
the pupil is dilated.
LIST OF ABBREVIATIONS
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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