Multiple cone visual pigments and the potential for trichromatic colour vision in two species of elasmobranch
1 Vision, Touch and Hearing Research Centre (Queensland Brain Institute),
University of Queensland, Brisbane, Queensland 4072, Australia
2 Department of Anatomy and Developmental Biology School of Biomedical
Sciences, University of Queensland, Brisbane, Queensland 4072,
Australia
* Author for correspondence (e-mail: n.hart{at}uq.edu.au)
Accepted 28 September 2004
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Summary |
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Key words: elasmobranch, microspectrophotometry, shovelnose ray, visual pigment, Rhinobatos typus, Aptychotrema rostrata, shark, vision
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Introduction |
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Cone photoreceptors mediate vision under bright light (photopic) conditions
when rod photoreceptor responses are saturated; the primary benefit of a
duplex retina is, therefore, to extend the range of light intensities over
which the visual system can operate
(Schultze, 1866). Since light
intensity varies by approximately 10 log10 units during the day,
from starlight to bright sunlight, it is not surprising that most vertebrates
possess duplex retinae (Walls,
1942
). However, in many vertebrates, cones also have a secondary
function, that is colour discrimination. If two or more cone types are
present, each containing a visual pigment with different spectral sensitivity,
the animal may be able to compare the outputs from these distinct cell types
and extract chromatic information from the retinal image.
At present, it is not known whether elasmobranchs have colour vision.
Physically restrained lemon sharks (Negaprion brevirostris) have been
conditioned to respond (signified by extension of their nictitating membrane)
when a coloured adapting light was silently substituted with another colour
(Gruber, 1975). However, the
results of this study were inconclusive as a significant difference in the
conditioned responses was only obtained when the change in stimulus colour was
accompanied by a change in stimulus brightness. Subsequent behavioural studies
employing a two choice discrimination paradigm also failed to demonstrate the
presence of colour vision in N. brevirostris (Gruber cited in
Cohen, 1980
). Furthermore,
there is no evidence for multiple cone types in lemon sharks based on the
available electrophysiological evidence
(Cohen and Gruber, 1977
;
Cohen, 1980
;
Cohen and Gruber, 1985
).
Nevertheless, the recent discovery in a jawless vertebrate, the lamprey
Geotria australis, of multiple cone types and visual pigment opsin
genes that are orthologous to the major classes of opsin genes found in jawed
vertebrates (Collin et al.,
2003a; Collin et al.,
2003b
), suggests that multiple cone visual pigments existed prior
to the divergence of the jawed and jawless vertebrate lineages and would have
been present in the ancestors of all elasmobranchs. Moreover, there are over
1100 extant species of elasmobranch and they occupy a diverse range of
habitats, from freshwater to marine, coastal to pelagic and shallow to deep
water. They share these niches with teleost fish, turtles and invertebrates
that are known to employ colour vision and it would be surprising if at least
some elasmobranch species did not share this visual ability. To this end, we
used microspectrophotometry to measure the spectral absorption of rod and cone
visual pigments in two species of predominantly shallow-dwelling elasmobranch,
the giant shovelnose ray Rhinobatos typus and the eastern shovelnose
ray Aptychotrema rostrata, and show for the first time that some
elasmobranchs do, in fact, have multiple cone types and, therefore, the
potential for colour vision.
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Materials and methods |
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Light and electron microscopy
Following an overdose of tricaine methane sulfonate salt (MS222; 1:2000),
four specimens of the giant shovelnose ray Rhinobatos typus Bennett
1830 (2568 cm total length) were sacrificed for light microscopical and
ultrastructural examination of the rod and cone photoreceptors. For light
microscopy, enucleated eyes were immersion fixed in 4% paraformaldehyde in 0.1
mol l1 phosphate buffer for 1 hbefore being dehydrated and
embedded in LR white resin (Sigma; Castle Hill, NSW, Australia). Sections (1
µm) were cut on an LKB ultramicrotome and stained with toluidine blue. For
electron microscopy, retinal tissue was fixed in 2% paraformaldehyde, 2.5%
glutaraldehyde in 0.1 mol l1 cacodylate buffer (pH 7.4) and
embedded in araldite before being sectioned on an LKB rotary ultramicrotome
(Collin et al., 1999).
Ultra-thin sections were stained with lead citrate and uranyl acetate, and
examined on either a Phillips 410 or a Phillips CM10 transmission electron
microscope set at 80 kV (Phillips Inc., Eindhoven, The Netherlands).
Microspectrophotometry
Two specimens of R. typus were caught in the shallows off Heron
Island, Great Barrier Reef, Queensland (23°26'S 151°55'E)
in May 2003. A third specimen was taken from shallow coastal waters off North
Stradbroke Island, Moreton Bay, Queensland (27°30'S
153°25'E) in February 2004. All specimens were newborn or
young-of-the-year females with a total length and disc width in the range
3947 cm and 1315 cm, respectively. Three adult specimens (total
length and disc width range 4276 cm and 1526 cm, respectively)
of the eastern shovelnose ray Aptychotrema rostrata Shaw and Nodder
1794 were also caught off North Stradbroke Island between October 2003 and
April 2004. Animals were kept in darkness overnight and killed with an
overdose of MS222 followed by spinal section and pithing.
Eye removal from dark-adapted animals and retinal dissection was conducted
under the illumination provided by a bank of 24 infra-red (IR) light emitting
diodes and visualized using an IR image converter (FJW Optical Systems Inc.,
Palatine, IL, USA) attached to one ocular of a stereo dissecting microscope.
Following enucleation, eyes were hemisected and immersed in an elasmobranch
Ringer solution (330 mmol l1 urea, 350 mmol
l1 NaCl, 4 mmol l1 KCl, 5 mmol
l1 CaCl2, 2 mmol l1
MgCl2; approximate osmolality 1050 mOsm kg1).
Small pieces (1 mm2) of retinal tissue were dissected away
from the vitreous and choroids, and transferred to a drop of Ringer solution
containing 10% dextran (MW 282,000; Sigma D-7265) placed in the middle of a
24x60 mm No. 1 glass coverslip. The retina was gently teased apart using
mounted needles, covered with an 18 mm diameter No. 0 coverslip and the edges
of the top cover slip sealed with nail varnish to prevent dehydration.
Transverse absorbance spectra (380800 nm) of cone and rod outer
segments were made using a computer-controlled, single-beam,
wavelength-scanning microspectrophotometer (MSP) described in detail elsewhere
(Hart, 2004). A sample scan
was made by aligning the measuring beam (typical dimensions 1x3 µm)
within a single outer segment and recording the amount of light transmitted at
each wavelength. A baseline scan was made in an identical fashion from a
cell-free area of the preparation adjacent to the measured cell. Baseline
transmittance was subtracted from that of the sample at each corresponding
wavelength to create a `pre-bleach' spectrum that was subsequently converted
to absorbance. Outer segments were then bleached with full spectrum `white'
light from the monochromator at its blaze angle for 3 min, and new sample and
baseline scans made to create a `post-bleach' spectrum. The post-bleach
spectrum was deducted from the pre-bleach spectrum to create a bleaching
difference spectrum for each outer segment. Visual pigment pre-bleach and
difference spectra were then analyzed as described elsewhere
(MacNichol, 1986
;
Govardovskii et al., 2000
;
Hart, 2002
) to obtain an
estimate of the wavelength of maximum absorbance (
max).
Spectroradiometry
Spectral radiance measurements were made using a calibrated,
computer-controlled Ocean Optics S2000 spectroradiometer (Ocean Optics,
Florida, USA) fitted with a 12 m ultraviolet-transmitting fibre-optic light
guide and a radiometric (32° acceptance angle) head. Measurements of
R. typus reef habitat were made on Heron Island reef flats and in the
Wistari channel, Great Barrier Reef, Queensland (23°27'S
151°54'E). Measurements of R. typus and A.
rostrata coastal/estuarine habitat were made off Amity Point, North
Stradbroke Island, Queensland (27°25'S 153°27'E). All
spectra were quantified in terms of photons rather than energy, as is
appropriate for the consideration of visual systems.
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Results |
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Photoreceptor morphology
The retinae of Rhinobatos typus and Aptychotrema rostrata
possess both rod and cone photoreceptors (Figs
1C and
2AD). Rods were
characterized by their relatively longer, cylindrical outer segments
(typically 2.03.5 µm in diameter and at least 20 µm in length),
narrower inner segments and smaller nuclei
(Fig. 2A). Cones were easily
distinguished from rods on the basis of their shorter, conical outer segments
and wider, tapering inner segments, which at the level of the myoid were
almost twice the width (6 µm) of the rods
(Fig. 2AC). Cone outer
segments, which were located at the level of the rod ellipsoid, were typically
48 µm in length and tapered from a width of 1.53.5 µm
nearest the inner segment to 12 µm at the tip. Unlike the rods, cone
outer segment discs were not surrounded by a plasma membrane
(Fig. 2D). Differences were
noted in the position of cone nuclei in the outer nuclear layer and the
alignment of their densely packed ellipsoidal mitochondria
(Fig. 2B,C), suggesting that
there are different morphological subtypes of cone.
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Microspectrophotometry
Microspectrophotometric data for both species of elasmobranch studied are
summarized in Table 1 and
Fig. 3. On the basis of
goodness-of-fit to mathematical visual pigment templates
(Govardovskii et al., 2000),
all absorbance spectra were considered to represent vitamin
A1-based visual pigments (rhodopsins). The retina of adult R.
typus contained a single type of rod, the outer segments of which
contained a medium-wavelength (`green') sensitive visual pigment with a mean
wavelength of maximum absorbance (
max) at 504 nm. The
retina of R. typus also contained a large number of cone
photoreceptors. Cone outer segments contained either a short-wavelength
(`blue') sensitive pigment with a mean
max at 477 nm, a
medium-wavelength (`green') sensitive pigment with a mean
max at 502 nm or a long-wavelength (`red') sensitive
pigment with a mean
max at 561 nm. The visual pigment
max values of a single juvenile R. typus caught
from estuarine waters off North Stradbroke Island (where the adult A.
rostrata were also caught) did not differ from those of juvenile R.
typus caught on the reef flats off Heron Island (Student's
t-test; rods: t=1.636, d.f.=14, P=0.124; short
wavelength-sensitive: t=0.674, d.f.=11, P=0.515;
medium wavelength-sensitive: insufficient data; long wavelength-sensitive:
t=1.023, d.f.=17, P=0.321) and so the data were pooled. The
retina of A. rostrata had morphologically similar rod and cone
photoreceptors to R. typus. However, the
max
values of the visual pigments in the rods (498 nm
max) and
the three cone types (459, 492 and 553 nm
max) in A.
rostrata were all at shorter wavelengths than the corresponding visual
pigment types in R. typus.
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Spectroradiometry
Spectral radiance along different lines of sight at different depths in
typical reef (R. typus) and coastal (both R. typus and
A. rostrata) waters are shown in
Fig. 4AD. At relatively
shallow depths in both habitats, there is a relatively broad range of
wavelengths available for vision (Fig.
4A,B; down-welling light), although wavelengths below 450 nm are
clearly more rapidly attenuated in coastal waters than on the reef. At 5 m in
the reef habitat, the down-welling light is still spectrally broad, although
the horizontal and up-welling radiances are significantly richer in short
wavelength light compared with shallow reef and deeper coastal waters
(Fig. 4C). By comparison, at
35 m in the greener coastal waters the spectral distribution of light
was quite uniform regardless of direction
(Fig. 4D).
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Discussion |
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Multiple cone types and the potential for colour vision
The majority of elasmobranchs studied have duplex retinae, although the
proportion of cones varies greatly between species. The presence of cones in
the retina of R. typus was shown previously by Collin
(1988), who reported a
relatively high peak rod to cone ratio of 4:1. Although no quantitative
analysis was performed in the present study, the retina of A.
rostrata also contained a high proportion of cones. The relative
abundance of cone photoreceptors and the presence of a highly mobile pupil
suggest that both species are well-adapted to brightly lit environments. The
morphology of the photoreceptors closely resembles that of other elasmobranch
species studied (Braekevelt,
1992
,
1994
). Cones were easily
distinguished from rods on the basis of their shorter, conical outer segments
and wider, tapering inner segments. Differences in the relative location of
cone nuclei in the outer nuclear layer and the alignment of their ellipsoidal
mitochondria suggests that there are several morphological subtypes of cone in
the shovelnose ray retina. In teleost fish
(Downing et al., 1986
) and
birds (Morris and Shorey,
1967
), different spectral cone types can be distinguished on the
basis of nuclear and ellipsoidal location. However, as we did not attempt to
correlate cone morphology with spectral type, further investigation is
required to confirm if this holds true for shovelnose rays and other
elasmobranchs.
Microspectrophotometric measurements revealed the presence of three
spectrally distinct cone visual pigments in both species of ray. The presence
of multiple cone types raises the possibility that these species have the
potential for trichromatic colour vision, a visual ability traditionally
thought to be lacking from elasmobranchs. A previous microspectrophotometric
and extraction spectrophotometric study on a closely related species, the
Atlantic guitarfish Rhinobatos lentiginosus, found only one rod
(max 496 nm) and one almost spectrally identical cone
visual pigment (
max 499 nm;
Gruber et al., 1991
). However,
it is quite possible that other cone types in R. lentiginosus were
missed: cones in both species of ray investigated in the present study were
often obscured by the surrounding rods and cone outer segments were easily
detached during preparation of the tissue. The only other
microspectrophotometric study performed on the elasmobranch retina failed to
obtain useful absorbance spectra from the cones of the two species
investigated, the brown smooth-hound (Mustelus henlei) and the
leopard shark (Triakis semifasciata), most probably due to the
paucity of cones in these bottom-dwelling species
(Sillman et al., 1996
).
Two other lines of evidence suggest that multiple cone types and colour
vision may be common in elasmobranchs, at least among the rays. Firstly,
electroretinographic recordings of the early receptor potential (ERP) in the
light-adapted retina of the common stingray (Dasyatis pastinaca)
revealed three peaks in spectral sensitivity at 476, 502 and 540 nm
(Govardovskii and Lychakov,
1977). As the ERP represents signals from the photoreceptors alone
(Brindley and Gardner-Medwin,
1966
), the three peaks in sensitivity can be correlated with the
presence of three spectrally distinct visual pigments. Secondly, horizontal
cells in the retina of the red stingray (Dasyatis akajei) have been
shown to possess colour-coded responses (C-type S-potentials) to chromatic
stimuli, hyperpolarizing when illuminated with short wavelength light and
depolarizing at longer wavelengths (Toyoda
et al., 1978
). Although C-type S-potentials are not necessary for
colour vision, they are only found in species that have a well-developed
colour sense, such as teleost fish (Stell
and Lightfoot, 1975
) and turtles
(Ammermüller et al.,
1995
).
Spectral tuning of rod and cone visual pigments
Interpreting the visual pigment spectral tuning characteristics of the two
species of shovelnose ray examined in this study is hampered by a lack of
life-history information, especially with regard to diurnal patterns in
activity and vertical migration through the water column. The rod and all
three types of cone found in R. typus have visual pigment
max values at longer wavelengths than the corresponding
cell types of A. rostrata. This is unexpected since the background
illumination in the typical coral reef habitat of R. typus,
especially at moderate depth, is characterized by a relative abundance of
short wavelength light compared with the more temperate coastal waters
inhabited by A. rostrata (Fig.
4AD). Shifts in cone
max that are
correlated with the spectral radiance of the water have been observed in a
number of teleost fish. For example, snappers (Lutjanidae) found in
the bluer waters of the outer Great Barrier Reef have cone visual pigments
with
max values shifted towards shorter wavelengths
compared to congeners occupying the greener waters of inshore reefs and
estuaries (Lythgoe et al.,
1994
).
It is also interesting that identical visual pigments
max values were found in both reef and coastal R.
typus. Other species of fish are known to show intraspecific variations
in visual pigment
max depending on the type of water they
inhabit (Shand et al., 2002
;
Jokela et al., 2003
). However,
because at least one of the visual pigments of R. typus would
coincide with the wavelength of peak transmission of the water in either
habitat, its visual system is perhaps equally well suited to reef and coastal
waters.
More information regarding both the spectral properties of habitat light and the behavioural biology of these species is required before further conclusions can be made. Nevertheless, it is evident that the visual ecology of many elasmobranchs is far more complex than once envisaged and is clearly a subject for further investigation. Whether or not the two species of shovelnose ray investigated in this study are capable of using their different cone types for colour discrimination is unknown but behavioural tests are currently underway in our laboratory.
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Acknowledgments |
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