Microspectrophotometry of visual pigments and oil droplets in a marine bird, the wedge-tailed shearwater Puffinus pacificus: topographic variations in photoreceptor spectral characteristics
Vision, Touch and Hearing Research Centre, School of Biomedical Sciences, University of Queensland, Brisbane, Queensland 4072, Australia
* e-mail: n.hart{at}uq.edu.au
Accepted 5 January 2004
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Summary |
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Key words: colour vision, MSP, microspectrophotometry, spectral sensitivity, petrel, shearwater, Puffinus pacificus, procellariiform, seabird, ocular media, visual ecology
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Introduction |
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Only 3% of the world's birds are classified as seabirds
(Nelson, 1980), but their
highly specialized life styles may provide some insights into avian retinal
design. However, while the optical structure of the eyes of marine species has
received considerable attention (Sivak,
1976
; Sivak et al.,
1977
,
1987
;
Martin and Brooke, 1991
;
Martin, 1998
,
1999
;
Martin and Prince, 2001
), only
limited and partial data are available on their photoreceptor spectral
sensitivities (Liebman, 1972
;
Bowmaker and Martin, 1985
;
Bowmaker et al., 1997
;
Ödeen and Håstad,
2003
). Described here are new data on the spectral absorption
characteristics of the visual pigments and cone oil droplets in the retinal
photoreceptors of the wedge-tailed shearwater Puffinus pacificus,
measured using microspectrophotometry. The wedge-tailed shearwater is a marine
pelagic species that spends most of its life on the open ocean, approaching
land only long enough to breed (Schodde
and Tidemann, 1997
). During the day, shearwaters forage low over
the sea's surface looking for fish, crustaceans and cephalopods. Although
predominantly diurnal in habit, they may come ashore after dark during the
breeding season (Warham,
1990
).
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Materials and methods |
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Microspectrophotometry of photoreceptors
Following enucleation, dark-adapted eyes were dissected in 340 mOsmol
kg1 phosphate-buffered saline (PBS; Oxoid, Basingstoke, UK)
and retinal tissue prepared for analysis with a microspectrophotometer as
described elsewhere (Hart et al.,
1998,
1999
,
2000a
,b
;
Hart, 2002
). Photoreceptors
were mounted in a solution of 340 mOsmol kg1 PBS containing
10% dextran (MW 282,000; Sigma D-7265). All preparations were conducted under
infrared (IR) illumination provided by a bank of IR light-emitting diodes
(LEDs) and visualized using an IR image converter (FJW Optical Systems Inc.,
Palatine, IL, USA).
The microspectrophotometer (MSP) used was a new field-portable single-beam wavelength-scanning instrument of simple design constructed by the author. The filament of a 12 V 50 watt tungsten halogen lamp was focused by a biconvex quartz lens (focal length f=50 mm) onto the entrance slit (1 mm width) of a Jobin-Yvon H10-61 UV-VIS monochromator (JY Horiba, France). The monochromator contained a directly driven, concave, holographic grating that dispersed the incident light and focused the diffracted wavefront onto the exit slit (1 mm width). An image of the exit slit was projected by another f=50 mm biconvex quartz lens onto a variable rectangular field aperture that controlled the dimensions of the measuring beam (minimum 1 µmx1 µm). Light passing through the aperture was linearly polarized to take advantage of the inherent dichroism of photoreceptor outer segments when illuminated side-on. An image of the aperture was demagnified and focused into the plane of a specimen on a micrometer-manipulated microscope stage using a Zeiss (Germany) x40 0.75 numerical aperture (NA) water immersion objective. Above the stage, a Leitz (Germany) x100 1.32 NA oil immersion objective imaged the measuring beam onto the photocathode of a photomultiplier tube (PMT; Model R928, Hamamatsu, Japan) or, via a sliding mirror that could be introduced to the beam path, onto the image plane of a black and white charge-coupled device (CCD) video camera. To view the specimen using the CCD camera, light (>900 nm) from an IR LED was directed into the beam path using a fixed 45° beamsplitter (19 mm diameter No. 0 coverglass; ProSciTech, Australia) positioned below the condenser objective.
To compensate for longitudinal chromatic aberration in the condenser objective, which would otherwise cause defocus of the measuring beam in the specimen plane when scanning through the spectrum (between 370 nm and 800 nm), a MIPOS 3 SG piezoelectric translator and 12 V 40 SG piezo amplifier (Piezosystem, Jena, Germany) were used to move the condenser automatically during the scan. The wavelength calibration of the MSP was checked with a calibrated Ocean Optics USB2000 spectroradiometer (Ocean Optics Inc., Dunedin, FL, USA) and was accurate to better than ±1 nm.
Sample and baseline scans were made from cellular and tissue-free regions of the preparation, respectively. Dimensions of the measuring beam varied from approximately 1 µmx1 µm for oil droplets and small cone outer segments to 2 µmx10 µm for rods. The photocurrent induced by light from the measuring beam reaching the photomultiplier was converted to a voltage by a transimpedance headstage amplifier (Hamamatsu C6271, Schizuoka, Japan) and differentially amplified to reject common-mode voltages. The voltage was further amplified and scaled to suit the input range of a 12-bit successive-approximation sample and hold analogue-to-digital converter that was subsequently interrogated by a Gateway laptop microcomputer via the parallel port. Each scan consisted of a `downward' long- to short-wavelength pass and an `upward' short- to long-wavelength spectral pass. Corresponding wavelength data from the downward and upward spectral passes were averaged together. To reduce the effects of in-scan bleaching, only one sample scan was made of a given outer segment and this was combined with a single baseline scan. Following these `pre-bleach' scans, outer segments were bleached with full spectrum `white' light from the monochromator for 3 min and an identical number of sample and baseline scans made subsequently. The `post-bleach' spectrum thus created was deducted from the pre-bleach spectrum to create a bleaching difference spectrum for each outer segment. To establish visual pigment-oil droplet pairings, the spectral absorptance of the oil droplet associated with the outer segment (if present) was also measured in the same way.
Analysis of visual pigment absorbance spectra
Baseline and sample data were converted to absorbance values at each
wavelength and spectra normalized to the peak and long-wavelength offset
absorbances determined by fitting a variable-point unweighted running average
to the data (Hart, 1998). A
regression line was fitted to the normalized absorbance data between 30% and
70% of the normalized maximum on the long-wavelength limb and the regression
equation used to predict the wavelength of maximum absorbance
(
max) following the methods of MacNichol
(1986
) and Govardovskii et al.
(2000
). Spectra from each
photoreceptor type that satisfied established selection criteria
(Levine and MacNichol, 1985
;
Hart et al., 1999
) were
averaged and reanalysed. For display, averaged spectra were overlaid with a
rhodopsin (vitamin A1-based) visual pigment template of the same
max generated using the equations of Govardovskii et al.
(2000
).
Analysis of oil droplet absorptance spectra
Sample and baseline data were converted to absorptance and normalized to
the maximum and long-wavelength offset absorptances obtained by fitting an
11-point unweighted running average to the data. Oil droplet absorptance
spectra were described by their cut-off wavelength (cut),
which is the wavelength of the intercept at the value of maximum measured
absorptance by the line tangent to the oil droplet absorptance curve at half
maximum measured absorptance (Lipetz,
1984a
). For comparison with other studies (e.g.
Partridge, 1989
) the
wavelength corresponding to half maximum measured absorptance
(
mid) was also calculated
(Lipetz, 1984a
).
Measuring spectral transmittance of the ocular media
The spectral transmittance (250800 nm) of the ocular media in the
anterior segment of the eye (cornea, aqueous humour and lens) was measured
along the optical axis using an Ocean Optics S2000 spectroradiometer. Broad
spectrum white light from an Ocean Optics PX-2 pulsed xenon lamp was delivered
to either the corneal or lenticular aspects of the anterior segment of a
hemisected eye at normal incidence using a 1 mm diameter fibre optic. The
anterior segment was supported on a hollow metal tube (10 mm in length and 5
mm internal diameter) screwed onto the sub-miniature type A (SMA) connector of
a 0.4 mm diameter fibre optic that relayed transmitted light to the S2000.
Data collection was controlled via a Toshiba laptop microcomputer.
After correcting the S2000 for electrical dark current, sample and baseline
readings were made with and without the anterior segment of the eye in
the beam path, respectively and converted to transmittance. In total,
13 spectra were obtained from the anterior segment of a single eye; of these,
six were illuminated from the corneal aspect and seven from the lenticular
aspect. All spectra were interpolated at 1 nm wavelength intervals, smoothed
using an 11-point unweighted running average and averaged together.
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Results |
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Microspectrophotometry
Microspectrophotometric data for visual pigments (Figs
2,
3) and oil droplets
(Fig. 4) measured outside the
visual streak are summarized in Table
1. The retina of the wedge-tailed shearwater contained five
different types of visual pigment in seven different classes of photoreceptor.
On the basis of goodness-of-fit to visual pigment templates
(Govardovskii et al., 2000),
all of the visual pigments were considered to be rhodospins, where the
chromophore is 11-cis retinal. Rods contained a medium-wavelength
sensitive (MWS) visual pigment with a
max at 502 nm. There
were four spectrally distinct types of single cone. Firstly, a violet
sensitive (VS) type with a 406 nm
max visual pigment and a
`transparent' T-type oil droplet that showed no significant absorptance down
to at least 370 nm. Secondly, a short-wavelength sensitive (SWS) type with a
450 nm
max visual pigment and a pale greenish-yellow C-type
oil droplet with a
cut at 445 nm. Thirdly, a MWS type with
a 503 nm
max visual pigment and a golden yellow Y-type oil
droplet with a
cut at 506 nm. Lastly, a long-wavelength
sensitive (LWS) type with a 566 nm
max visual pigment and a
red R-type oil droplet with a
cut at 562 nm. Both the
principal and accessory members of the double cone pair contained the same 566
nm
max visual pigment that was also found in the LWS single
cones. While the accessory member did not contain an oil droplet, the
principal member had a colourless oil droplet with a
cut at
413 nm.
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In the central retina, cone oil droplets appeared either
transparent/colourless or pale green (Fig.
1C). The transition from `normally' pigmented oil droplets located
towards the periphery (Fig. 1A)
to these less pigmented types in the centre of the visual streak occurred over
a short distance (approximately 50 µm when measured on a flat-mounted
retina) on the edges of the visual streak (Figs
1B,
5A). Unlike in the periphery,
definitive visual pigment-oil droplet pairings in the central retina/visual
streak could not be made because of the smaller size of the cone outer
segments (<1 µm diameter where present) and the fact that the retinal
tissue was not dispersed in order to preserve orientation. Nevertheless, it is
likely that there were several different types of cone in the central retina,
each of which contained a different visual pigment, because there were oil
droplets of slightly different diameters
(Fig. 1C) and with different
spectral absorptance characteristics (Fig.
5B).The absorptance spectra of oil droplets measured in the
central retina fell into five distinct groups (labeled t, c,
y, r and p in Fig.
5B). The most common droplet type (p) had a spectral
absorptance (mean cut=414 nm, N=12) that closely
resembled the P-type oil droplets of the principal member of the LWS double
cones in the peripheral retina. Transparent oil droplets (t) showing no
significant absorption across the spectrum were also present, and were
identical to the T-type oil droplets associated with the VS visual pigment in
the periphery. The remaining three types of oil droplet were classified as
c, y and r and were considered to be less pigmented
versions of the C-, Y- and R-type oil droplets found in the SWS, MWS and LWS
single cones at the periphery. This was deduced by taking the measured
absorptance spectra for the central c, y, and r oil
droplets (Fig. 5B) and modeling
the effect of increasing the density of the carotenoid pigment(s) they contain
to levels estimated for the C, Y and R-type oil droplets found in the
periphery. The results of this modeling are shown in
Fig. 5C. Peak absorbances for
the peripheral Y- and R-type oil droplets (16.6 and 2.4, respectively) were
estimated from their
cut values using the equations given
by Lipetz (1984b
) for turtle
oil droplets. The relationship between C-type oil droplet
cut and peak absorbance has not been quantified and was
taken to be 1.0 for peripheral C-type oil droplets; this value is the lower
limit for pigmented droplets in the turtle retina
(Lipetz, 1984b
). (The peak
absorbance of densely pigmented oil droplets cannot be measured accurately
with a microspectrophotometer due to the effects of bypassing light
(Lipetz, 1984b
), which in the
current machine limit the upper absorbance values that can be measured to
about 0.9 for a 3 µm diameter droplet, as indicated by the flat-topped
absorptance spectra for the C-, Y- and R-type oil droplets in
Fig. 4A.) Smoothed absorptance
spectra for the central c, y, and r oil droplets were
converted to absorbance, scaled by a factor equivalent to the ratio of central
(measured) oil droplet absorbance to peripheral (estimated) oil droplet
absorbance (3.2, 8.5 and 60.3 for the C:c, Y:y and R:r
types, respectively) and converted back to absorptance for display. The
modeled oil droplets, labeled c', y' and
r' in Fig. 5C,
resemble the peripheral C-, Y- and R-type droplets, having
cut at around 445, 490 and 540 nm, respectively. From Figs
5A,C and
1AC it seems more than
likely that, rather than losing particular cone types, the oil droplets
associated with the SWS, MWS and LWS visual pigments gradually reduce their
carotenoid pigmentation the nearer they are to the centre of the visual
streak.
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Cone quantal sensitivities
With the exception of the transparent T-type oil droplet associated with
the VS (or UVS) single cones, avian cone oil droplets generally act as
long-pass cut-off filters. Consequently, the spectral sensitivity of a given
cone is the product of the spectral absorptance of the visual pigment in the
outer segment and the spectral transmittance (1-absorptance) of the oil
droplet with which it is paired. Relative quantal spectral sensitivities were
calculated for single cone photoreceptors in different regions of the
wedge-tailed shearwater retina (Fig.
7A,B), as follows. Visual pigment spectral absorptance was modeled
using mathematical templates (Govardovskii
et al., 2000) of the appropriate
max
(Table 1). Outer segments were
assumed to be 16 µm long (Morris and
Shorey, 1967
) and contain a visual pigment with a specific
(decadic) absorbance of 0.014 µm1
(Bowmaker and Knowles, 1977
).
Predicted photon catches for each cone type were also adjusted according to
the cross-sectional area of the relevant oil droplet they contained
(Table 1) and the transmittance
of the ocular media (Fig. 6).
For cones in the peripheral retina (i.e. outside the visual streak;
Fig. 1A), the VS, SWS, MWS and
LWS cone visual pigments were combined with their corresponding oil droplets,
the absorptance spectra of which are labeled T, C, Y and R, respectively, in
Fig. 4A. Because the T-type oil
droplets do not contain short-wavelength-absorbing carotenoid pigments, the
peak sensitivity of the VS cone (407 nm) is very similar to the
max of the visual pigment it contains. However, spectral
filtering by the C-, Y- and R-type oil droplets shift the peak spectral
sensitivities of the SWS, MWS and LWS single cones (472, 538 and 600 nm,
respectively; Fig. 7A) to
wavelengths longer than the
max of their respective visual
pigments.
|
In the central retina, the VS, SWS, MWS and LWS single cones were assumed
to contain the t, c, y and r droplets shown in
Fig. 5B (see above). Calculated
spectral sensitivities are also displayed in
Fig. 7A. The spectral location
of the peak sensitivity of the VS single cone was the same as in the
periphery. However, the reduced pigmentation of the presumptive C-, Y- and
R-type oil droplets in the centre of the visual streak results in smaller
shifts in the peak sensitivities of the SWS, MWS and LWS single cones towards
long wavelengths (466, 512 and 573 nm, respectively). The length of the cone
outer segments was assumed to be identical between central and peripheral
regions, as appears to be the case for other bird species (e.g.
Rojas et al., 1999).
Nevertheless, the total photon catch of all single cone types in the centre of
the visual streak was less than that at the periphery because of the reduced
cross sectional area of the oil droplets (mean diameters 1.4, 2, 2 and 2.1
µm for t, c, y and r oil droplets,
respectively), despite the reduction in oil droplet pigmentation (which at the
periphery reduces the overall photon catch of the outer segment by 30, 47 and
39%, respectively, for the SWS, MWS and LWS single cones). To further
illustrate the transition in cone spectral properties from peripheral to
central retina, the spectral sensitivities of LWS single cones on the edge of
the visual streak were also calculated
(Fig. 7B, traces 14),
using the absorptance spectra for oil droplets that changed from red to orange
in this retinal area (Fig. 5A,
spectra 14).
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Discussion |
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With a max at 406 nm, the VS visual pigment of the
wedge-tailed shearwater is similar to the only other marine birds for which
data are available, the Manx shearwater Puffinus puffinus (402 nm
max; Bowmaker et al.,
1997
) and the Humboldt penguin Spheniscus humboldti (403
nm
max; Bowmaker and
Martin, 1985
). This type of VS visual pigment, which differs
subtly from those found in anseriform and galliform species
(
max 415426 nm), is also found in the ostrich
Struthio camelus (405 nm
max;
Wright and Bowmaker, 2001
) and
the feral pigeon Columba livia (409 nm
max;
Bowmaker et al., 1997
) and so
is not exclusive to marine bird species. On the basis of SWS1 opsin DNA
sequences, Ödeen and Håstad
(2003
) have suggested that the
distribution of UVS/VS visual pigment
max values among bird
species is complex and probably reflects ecological adaptations rather than
phylogenetic relatedness, as seems to be the case for cone photoreceptor
abundance (Goldsmith et al.,
1984
; Partridge,
1989
; Hart,
2001a
). There are likely to be many different adaptive reasons for
a particular complement of photoreceptor spectral sensitivities, depending,
for example, on the physical habitat and foraging or predator avoidance
behaviours of a given species.
As an oceanic marine bird, the visual system of the wedge-tailed shearwater
appears to be well adapted to its photic environment. Shearwaters use a
variety of strategies to capture their prey, which consists largely of fish,
squid and crustaceans (Nelson,
1980), but feed mainly while floating on the water or during
shallow dives made either from the surface or a short distance above it
(Warham, 1990
). They must,
therefore, be able to detect their prey through the airwater interface,
although this is a complex visual task: plunge-diving birds most cope not only
with the effects of refraction on the apparent position of the prey item
underwater (Katzir, 1993
), but
also with specular reflection of skylight from the surface that interposes a
contrast-reducing glare (Lythgoe,
1979
). Reflections from the surface of the water have the same
spectral distribution as skylight, but the spectral radiance of the upwelling
light from the ocean against which prey must be detected is
dominated by the absorption and scatter of the water
(Austin, 1974
). Considering
this phenomenon, Lythgoe
(1979
) proposed that a visual
system most sensitive to wavelengths in which the upwelling light is rich, and
the surface reflectance relatively poor, would be adaptive for through-surface
vision.
The spectral distribution of upwelling light from a body of water depends
on the amount of particulate matter, dissolved organic compounds and
chlorophyll it contains. Different types of water have different levels of
these substances and, accordingly, different upwelling spectral radiances or
`colours' (Austin, 1974;
Jerlov, 1976
).
Fig. 8 shows the calculated
difference between upwelling and surface-reflected radiances for three
different water types: `blue', `blue-green' and `green', calculated from data
in Austin (1974
). The
geographical range of the wedge-tailed shearwater extends throughout the
tropical and subtropical Indian and Pacific Oceans
(del Hoyo et al., 1992
).
Consequently, they forage mainly over oceanic `blue' water types (Jerlov types
I, IA and IB; Jerlov, 1976
)
whose upwelling spectral radiance is relatively richer in short wavelengths
between about 400 and 500 nm (Fig.
8). Below 400 nm, submerged objects would become increasingly
difficult to distinguish against the surface glare and the 406 nm
max VS visual pigment of the wedge-tailed shearwater would,
therefore, be more useful than a UVS-type visual pigment
(
max<400 nm) for through surface vision. It is also
interesting to note that the proportion of VS cones in the wedge-tailed
shearwater retina (approximately 16% of all cone types) is at least twice as
high as in many terrestrial bird species (e.g.
Goldsmith et al., 1984
; Hart et
al., 1998
,
2000b
;
Wright and Bowmaker, 2001
) and
marine species (e.g. silver gull Larus novaehollandiae, noddy tern
Anous minutus) that surface seize but do not plunge dive
(Hart, 2001a
). Moreover,
despite their suggested role in movement detection
(Campenhausen and Kirschfeld,
1998
), the retinae of blue-water marine birds generally contain a
lower proportion of double cones (wedge-tailed shearwater 34%, silver gull
30%, noddy tern 29%) compared to terrestrial species (range 3556%;
Hart, 2001a
), possibly because
their long-wavelength sensitivity is less useful for through-water vision.
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The LWS visual pigment of the wedge-tailed shearwater has a similar
max (566 nm) to other terrestrial bird species (see
Hart, 2001b
) and is not
shifted towards shorter wavelengths as in the Humboldt penguin Spheniscus
humboldti (Bowmaker and Martin,
1985
). The 543 nm
max LWS visual pigment of the
penguin is presumably an adaptation to the restricted spectral bandwidth it
encounters when foraging in the ocean at depths of 30 m or more
(Williams, 1995
), where longer
wavelengths are attenuated more rapidly than shorter wavelengths with
increasing depth (Jerlov,
1976
). Plunge-diving shearwaters, on the other hand, take most of
their prey within 2 m of the surface
(Warham, 1990
) where the
spectral distribution of light available for vision is less restricted.
The wedge-tailed shearwater retina has a distinct area centralis
horizontalis or visual streak running horizontally across the retina. A
similar band of increased cell density with or without a central fovea
has been shown, either anatomically or ophthalmoscopically, in several
other procellariiform species: the sooty albatross Phoebetria fusca,
shy albatross Diomedea cauta, Manx shearwater Puffinus
puffinus, sooty shearwater Puffinus griseus, soft-plumaged
petrel Pterodroma mollis, Fulmar petrel Fulmaris glacialis
and giant petrel Macronectes giganteus
(Wood, 1917;
O'Day, 1940
;
Lockie, 1952
;
Hayes and Brooke, 1990
). Some
shearwaters, for example the little shearwater Puffinus assimilis,
lack a visual streak and instead have a simple area centralis;
differences in the retinal topography of petrel species are undoubtedly
related to visual ecology, most likely feeding behaviour
(Hayes and Brooke, 1990
).
Several specialized functions have been attributed to linear areas in birds
and other animals, including movement detection, spatial orientation and
fixation of the horizon (reviewed in
Meyer, 1977). Measurements of
the visual fields of the Manx shearwater eye reveal that the long axis of the
visual streak is aligned parallel to the physical horizon
(Martin and Brooke, 1991
), as
is the case for other animals that inhabit open, relatively featureless
environments (Hughes, 1977
;
Meyer, 1977
). The region of
visual space from just above the horizon to just below it will be of great
significance to birds such as shearwaters in finding food. Shearwaters usually
forage within 10 m of the water's surface
(Haney et al., 1992
) and
search for prey solitarily, only converging to form flocks when a source of
food is located and an individual is observed dropping to the surface to feed
(Warham, 1990
). Haney et al.
(1992
) calculated that the
mean horizontal distance over which procellariiform seabirds were recruited
visually to a feeding flock was around 4.5 km and even proposed a theoretical
limit of 2030 km. It is evident, therefore, that a visual streak
sampling the physical horizon with a high spatial resolving power would be
adaptive for the detection of potential food sources on the open ocean.
The most intriguing feature of the wedge-tailed shearwater retina is that
the pigmented cone oil droplets lose their coloration in the central area of
the visual streak. These pale-coloured oil droplets in the visual streak are
of marginally different sizes (Fig.
1C) and have slightly different absorptance spectra
(Fig. 5B). Moreover, the
transition from brightly coloured to almost colourless droplets can be seen at
the edge of the visual streak (Figs
1B,
5A). It seems likely,
therefore, that rather than only one cone type being present at the centre of
the visual streak, all different types of cone are present, but contain oil
droplets with absorptance spectra that are different from those in the
peripheral retina. This has also been observed in other species that have very
small, densely packed photoreceptors in their central retina, e.g. sacred
kingfisher Todiramphus sanctus
(Hart, 2001a) and laughing
kookaburra Dacelo novaeguineae (N. S. Hart, unpublished). Pigmented
oil droplets act as long-pass cut-off filters, blocking almost all light below
a critical wavelength (
cut). Consequently, the effect of a
coloured oil droplet on a given cone type is to narrow its spectral
sensitivity function, shift the peak sensitivity to a wavelength longer than
the
max of the visual pigment it contains and reduce the
overall photon catch (Bowmaker,
1977
). From the predicted spectral sensitivities of the cone
photoreceptors in the wedge-tailed shearwater retina
(Fig. 7A), it is evident that
the reduction of spectral filtering by oil droplets in the central retina
results in greater overlap between adjacent spectral classes and a shift in
the peak sensitivity of the SWS, MWS and LWS single cone types towards shorter
wavelengths compared to those at the periphery. Reduced overlap of adjacent
cone spectral sensitivities is thought to improve the discrimination of
broadband (`natural') reflectance spectra and enhance colour constancy
(Govardovskii, 1983
; Vorobyev,
1997
,
2003
;
Vorobyev et al., 1998
).
However, the benefits of spectral filtering by oil droplets are strongly
dependent on light intensity because they reduce the overall quantum catch of
the cone and, accordingly, increase photoreceptor signal noise. In the
wedge-tailed shearwater retina, the cones become narrower and more densely
packed with decreasing eccentricity (Fig.
1), presumably to enhance spatial acuity in the visual streak. The
associated decrease in photon capture area results in a lower quantal
sensitivity compared to peripheral cones
(Fig. 7A), despite the
reduction in oil droplet pigmentation. Moreover, ganglion cells in retinal
regions of high spatial acuity, such as the visual streak, tend to have
smaller receptive fields (Rodieck,
1973
), receive inputs from fewer cones (e.g. Manx shearwater;
Lockie, 1952
) and,
consequently, have a lower signal-to-noise ratio than ganglion cells in the
periphery. Theoretical models suggest that the benefit of coloured oil
droplets for colour discrimination is marginal at lower light intensities
(Vorobyev, 2003
). This
trade-off between spatial acuity (small cones, low summation) and contrast
sensitivity (big cones, high summation) may preclude the presence of highly
pigmented oil droplets in centrally located cones because they would further
reduce quantum catch below a particular noise threshold. This is probably also
the reason why nocturnal and crepuscular species of bird do not have highly
pigmented droplets (Muntz,
1972
; Bowmaker and Martin,
1978
).
If, as in chickens Gallus gallus
(Osorio et al., 1999), outputs
from the four single cone types in the wedge-tailed shearwater retina are
compared using opponent mechanisms in a tetrachromatic colour vision system, a
coloured object whose image falls on the photoreceptors in the visual streak
will produce different cone opponent signals than if it fell on the peripheral
retina, especially if its reflectance is rich in short wavelengths of light.
Whether or not the neural circuitry of the opponent mechanisms compensates for
this topographic variation in colour perception is unknown and this is clearly
an area for future study.
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List of abbreviations |
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Acknowledgments |
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References |
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