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First published online November 17, 2006
Journal of Experimental Biology 209, 4776-4787 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02568
Cone photoreceptor oil droplet pigmentation is affected by ambient light intensity
Vision, Touch and Hearing Research Centre, School of Biomedical Sciences, University of Queensland, Brisbane, Queensland 4072, Australia
* Author for correspondence (e-mail: n.hart{at}uq.edu.au)
Accepted 2 October 2006
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: microspectrophotometry, avian colour vision, carotenoid, photon catch, spectral tuning
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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), located in the ellipsoid at the distal end of the inner
segment. Usually, the oil droplet completely covers the entrance aperture of
the outer segment, and most of the incident light passes through it before
reaching the visual pigment (Wortel and
Nuboer, 1986). The oil droplets found in the photoreceptors of
some species of chondrostean fishes (Walls
and Judd, 1933), anuran amphibians
(Hailman, 1976), geckos
(Ellingson et al., 1995),
monotremes (Walls, 1942) and
marsupials (O'Day, 1935;
Arrese et al., 2002;
Arrese et al., 2005) do not
have obvious pigmentation. The cone oil droplets of birds, turtles, lizards
and the Australian lungfish, however, have a pale green, greenish yellow,
golden yellow or ruby red colouration, depending on the spectral identity of
the cone and the species (Walls and Judd,
1933; Robinson,
1994; Bailes et al.,
2006).
Avian oil droplets are the best studied, with all but one spectral type
containing high concentrations of diet-derived, short-wavelength-absorbing
carotenoid pigments (Goldsmith et al.,
1984; Davies,
1985). Birds possess a single type of medium-wavelength-sensitive
(MWS) rod, four spectrally distinct types of single cone and a single type of
double cone (for reviews, see Hart,
2001; Hart and Hunt, in press). Single cones containing an
ultraviolet-(UVS) or violet-sensitive (VS) visual pigment [SWS1 opsin; for
terminology see (Yokoyama,
2000)] have a non-pigmented `T-type' oil droplet, with no
significant absorption of wavelengths between at least 330 and 800 nm. Single
cones expressing a short-wavelength-sensitive (SWS) visual pigment (SWS2
opsin) in their outer segment have a `colourless' or pale green `C-type' oil
droplet. The cut-off wavelength, or 
cut
(Lipetz, 1984), of the C-type
oil droplet in different bird species varies from 392 to 444 nm. Single cones
containing a MWS visual pigment (RH2 opsin) have a golden yellow Y-type oil
droplet (cut = 505-516 nm), and those containing a
long-wavelength-sensitive (LWS) visual pigment (M/LWS opsin) have a red R-type
oil droplet (cut = 552-586 nm). The outer segments of both
the principal and accessory members of the double cone pair contain the same
LWS visual pigment found in the LWS single cones. Usually, only the principal
member of the double cone contains an oil droplet (P-type), but a smaller
droplet (A-type) might occasionally be seen in the accessory member
(Bowmaker et al., 1997;
Hart et al., 1998). The P-type
oil droplet might appear colourless, pale green, greenish yellow or yellow
depending on the spectral location of the cut (range =
407-489 nm). Avian rods do not contain oil droplets.
The incorporation of pigmented compounds into the oil droplet creates an
intracellular spectral filter that has a marked effect on the spectral
sensitivity of the cone (Neumeyer and
Jäger, 1985; Wortel and
Nuboer, 1986). For example, in the case of avian MWS and LWS
single cones, calculations show that absorption of short wavelengths by the Y-
and R-type oil droplets will shift the wavelength of peak sensitivity of the
cones approximately 40 nm towards longer wavelengths (540 nm and 605 nm,
respectively) and reduce the sensitivity of the outer segment by 50% or more
(Bowmaker and Knowles, 1977;
Hart and Vorobyev, 2005). For
all cone types, the absorption of short wavelengths by the pigmented oil
droplets narrows the spectral sensitivity function of the photoreceptor and
reduces the overlap between adjacent spectral classes, potentially improving
the discrimination of broadband (i.e. natural) reflectance spectra
(Govardovskii, 1983;
Vorobyev, 1997;
Vorobyev et al., 1998;
Vorobyev, 2003) and enhancing
colour constancy (Dyer,
2001).
Nocturnal birds also have coloured cone oil droplets, but they are less
densely pigmented than those of diurnal species. The tawny owl (Strix
aluco) has dark yellow, pale yellow and pale red oil droplets
(Bowmaker and Martin, 1978),
whereas the tawny frogmouth (Podargus strigoides) lacks red oil
droplets altogether and has only yellow, pale green and transparent oil
droplets (N.S.H., unpublished observations). The reduced pigmentation of oil
droplets in nocturnal species suggests that, at low light levels, heavily
pigmented oil droplets either are of no use or reduce photon capture
sufficiently to be a hindrance to vision.
While the reduction in oil droplet pigmentation over evolutionary time might have occurred as a result of genetic selection for individuals that were better able to see and thus survive under nocturnal or crepuscular lighting conditions, short-term phenotypic changes in oil droplet pigmentation might also be adaptive for optimising visual performance under different environmental conditions. To investigate this possibility, we have used microspectrophotometry to measure objectively the spectral absorptance characteristics of the cone oil droplets of chickens reared under either bright or dim light.
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Materials and methods |
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After a further 2 weeks (i.e. at 4 weeks of age) the chicks were divided randomly into two treatment groups, designated as `bright' light (N=9) and `dim' light (N=9), for the remainder of the experiment. Each group was placed into one of two large outdoor mesh cages (4 x 3 x 2 m, length x width x height, respectively) with bare earth floors. The cages were adjacent to each other and partially shaded by nearby eucalyptus trees. Both cages had a 1.5x1.5 m waterproof (corrugated steel) shade roof in the north-east corner. Over the experimental period, both cages had the same minimum and maximum recorded ambient temperatures of 12°C and 36°C, respectively. The only difference between the two treatments was that the cage housing the dim light group of chicks was covered on all sides and over the roof by a single layer of closely woven black plastic weed matting (Mitre 10, Brisbane, Australia) secured to the cage mesh and further shaded by an opaque plastic tarpaulin (6x4 m) suspended 1 m above the cage. The characterisation of the intensity and spectral distribution of the ambient light in each of the treatment cages is described in the next section.
Both groups had access to a covered wooden chicken coop and were provided with straw for bedding. Food and water were provided ad libitum throughout the experiment. Up to 4 weeks of age, the feedstock was Riverina Chick Starter Crumbles (Riverina Australia Pty. Ltd, Brisbane, Australia), which is derived predominantly from wheat grains. Thereafter, chicks were fed SupaStok Coarse Grain Mix (Ridley AgriProducts Pty. Ltd, Pakenham, Australia), which on the basis of mass consists of 26% sorghum, 26% wheat, 26% corn, 8% barley, 3% sunflower seeds and 11% other ingredients. No artificial carotenoid supplements were provided.
Spectroradiometry and photometry
Spectral irradiance in each of the treatment cages was recorded using a
calibrated, computer-controlled Ocean Optics S2000 charge-coupled device (CCD)
spectroradiometer (Ocean Optics Inc., Dunedin, FL, USA) connected to an Ocean
Optics CC3-UV cosine-corrected irradiance probe by a 12 m long, 1 mm diameter,
UV-visible-transmitting fibre optic. The probe was positioned 50 cm above the
ground (approximately the head height of an adult chicken) in the centre of
each cage and measurements were made (N=5) with the probe pointing
both directly upwards and directly downwards to record the downwelling and
upwelling radiation impinging upon the ventral and dorsal retinal surfaces of
the chickens' eyes, respectively.
Measurements of illuminance (lux) were also made using a calibrated, hand-held light-meter (Lutron LX-107HA; Lutron Electronic Enterprise Co. Ltd, Taipei, Taiwan). Unlike the spectral irradiance measurements, lux measurements are based on human photopic spectral sensitivity functions, but they are useful for comparison with previous studies in which light intensities have been measured in lux (lx). The recording probe was positioned 50 cm off the ground and measurements were made from five different locations within the cage (once in each corner and in the centre) with the probe pointing both directly upwards and directly downwards. All measurements were made at the end of the experimental period and were taken under full sunlight at approximately midday.
Microspectrophotometry
Chickens were euthanised with an overdose of sodium pentobarbitone
(Lethabarb, Virbac Australia Pty. Ltd, Peakhurst, Australia), followed by
cervical dislocation and weighed using an electronic balance (accuracy
±1 g). The left eye from each chicken was removed and bisected at the
equator, immediately anterior to the ora terminalis. Only the left
eye was used so as to standardise the sampling procedure and avoid introducing
errors caused by differences in the way in which the left and right eyes might
be dissected. This is important because oil droplet spectra vary subtly
depending on retinal location and there is also some evidence to suggest that
the proportions of cone photoreceptors vary between the left and right retinae
of the same bird (Hart et al.,
2000). The posterior segment of the globe containing the retina
was immersed in cold (4°C) phosphate-buffered saline (167 mmol
l-1 NaCl, 3 mmol l-1 KCl, 10 mmol l-1
Na2HPO4, 2 mmol l-1
KH2PO4; osmolality 340 mosmol kg-1; pH 7.3;
Oxoid Ltd, Basingstoke, UK) and the vitreous dissected away. Two samples of
neural retina approximately 2x2 mm were cut from the fundus, both with
their peripheral edge a distance of 1 mm from the ora terminalis. The
first piece was taken from the ventral peripheral retina, 2 mm nasal to the
base of the pecten; the second piece was removed from the dorsal peripheral
retina exactly opposite the site of the ventral sample. Each piece of retinal
tissue was transferred to a drop of glycerol (APS Finechem, Seven Hills,
Australia) placed in the centre of a 24x60 mm No. 1 glass coverslip and
the retina oriented with the photoreceptor layer uppermost. The preparation
was then covered with a 22x22 mm No. 0 glass coverslip, blotted gently
with filter paper to remove excess glycerol and the edges of the top coverslip
sealed with nail varnish to prevent movement of the retina. Preparations were
stored in a refrigerator at 4°C for up to 6 h before use.
Transverse absorptance spectra (330-800 nm) of cone photoreceptor oil
droplets were made using a computer-controlled, single-beam,
wavelength-scanning microspectro-photometer (MSP) described in detail
elsewhere (Hart, 2004). A
sample scan was made by aligning the measuring beam (dimensions 1x1
µm) within an oil droplet and recording the amount of light transmitted at
each wavelength across the spectrum. 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 single baseline-corrected scan that was
subsequently converted to absorptance. Absorptance spectra were obtained from
at least 10 different oil droplets for each cone class that contains a
pigmented oil droplet in both the dorsal and ventral retinal samples. The
so-called `transparent' T-type oil droplets found in the VS single cones were
not measured. The diameter of each droplet measured was recorded (to an
accuracy of ±0.25 µm) with the use of a calibrated acetate sheet
placed over an image of the retina, supplied by a CCD camera attached to the
MSP, projected onto a television screen. One chicken from each treatment group
was sampled at intervals from 10 to 33 weeks of age (i.e. from 6 to 29 weeks
of treatment under the different lighting regimes). In a given sampling week,
chickens from different light-treatment groups were measured on different days
but within 5 days of each other.
Analysis of oil droplet absorptance spectra
Oil droplet absorptance spectra were normalized to the maximum, and
long-wavelength offset absorbances obtained by fitting an 11-point unweighted
running average to the data. Spectra were then described by their cut-off
wavelength, cut, as defined by Lipetz
(Lipetz, 1984). Briefly, a
tangent line was fitted (see below) to the long-wavelength limb of the
normalized absorptance spectrum and the cut calculated as
the wavelength at which the tangent line had a value of 100% normalized
absorptance. The cut is particularly useful as an objective
measure of oil droplet pigmentation because it is directly related to
carotenoid concentration (Lipetz,
1984; Hart and Vorobyev,
2005). For the C-, Y- and R-type single cone oil droplets, the
tangent line was fitted using absorptance values on the long-wavelength limb
between 70% and 30% of the normalized maximum. For double cone P-type oil
droplets displaying a secondary peak in the long-wavelength limb of their
absorptance spectrum, the tangent line was fitted using different absorptance
value ranges, as follows: where the secondary peak was less than 50% of the
normalized maximum, the tangent line was fitted using absorptance values
between 70% and 60% of the maximum; where the secondary peak was more than or
equal to 50% of the normalized maximum, the tangent line was fitted using
absorptance values between 40% and 30%.
Modelling the spectral sensitivity of cone outer segments
The relative quantal spectral sensitivity of the outer segments of the SWS,
MWS and LWS single cones and the principal member of the LWS double cones in
the ventral retina of the bright-light and dim-light groups was modelled as
described previously (Hart,
2002; Hart, 2004;
Hart and Vorobyev, 2005). Cone
outer segment absorptance was modelled using the rhodopsin (vitamin
A1-based) visual pigment templates of Govardovskii et al.
(Govardovskii et al., 2000), a
specific (decadic) absorbance of 0.014 µm-1
(Bowmaker and Knowles, 1977)
and a cone outer segment length of 16 µm
(Morris and Shorey, 1967).
Microspectrophotometrically measured oil droplet absorptance spectra recorded
from the last chicken sampled (after 29 weeks of light treatment, i.e. 33
weeks of age) in each treatment group were fitted with an 11-point running
average, corrected for any long-wavelength absorptance offset, converted to
transmittance and normalized. Spectral sensitivity was defined as the product
of outer segment axial absorptance and oil droplet transmittance.
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cut or mean diameter was
significantly correlated with time (weeks of light treatment) for each of the
different pigmented oil droplet types, in both the dorsal and ventral retina
of the dim-light and bright-light groups. Subsequently, the data were split
into juvenile (
18 weeks of age) and adult (
24 weeks of age) sets
(Limburg, 1975). Trends in
mean cut value and mean diameter for the different oil
droplet types across treatment groups and between dorsal and ventral retinal
regions in both juveniles and adults were analysed using a General Linear
Model (GLM), with body mass as a covariate. The effect of light treatment on
body mass was analysed using a two-sample t-test. Statistical
analyses were performed with the aid of Minitab 14.20 (Minitab Inc., State
College, PA, USA). |
Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Microspectrophotometry
Absorptance spectra of the different types of pigmented oil droplets found
in the retinal cone photoreceptors of 33-week-old chickens are shown in
Fig. 2. These spectra are
similar to those obtained for the chicken by Bowmaker and Knowles
(Bowmaker and Knowles, 1977)
and Bowmaker et al. (Bowmaker et al.,
1997), although there are distinct differences in the absorption
spectra of specific droplet types depending on retinal location and
light-treatment group. These differences are also evident in
Fig. 3, in which mean oil
droplet cut-off wavelength (cut) is plotted against weeks
of treatment for both bright-light and dim-light groups.
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cut values and/or the diameters of the oil droplets were
significantly correlated with time (Table
1). For all significant relationships found, the correlation was
positive, i.e. oil droplet diameter and cut tended to
increase with age. In view of these correlations, and because other retinal
characteristics - such as the relative proportions of the different oil
droplet types [Pézard, cited in Meyer
(Meyer, 1977)] - are reported
to be affected by the state of maturity, the data were split into juvenile and
adult sets for subsequent analyses.
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In juvenile chickens, the cut values of the Y-, R- and
P-type oil droplets in the bright-light group were at longer wavelengths than
those in the dim-light group, although the difference was significant only for
the P-type droplets (Tables 2,
3;
Fig. 3). In adult chickens,
however, all pigmented oil droplet types, regardless of retinal location, had
cut values shifted significantly towards longer wavelengths
and were therefore more densely pigmented in the group reared in bright light
compared with the group reared in dim light (Tables
2,
4;
Fig. 3). The absolute shift in
cut for the C-type droplets was smaller than for the other
droplet types (Table 2), which
might reflect the fact that the light intensity in light-treatment groups
differed less at short wavelengths (<400 nm) than at other regions of the
spectrum (Fig. 1B) to which the
chickens would be sensitive (Fig.
4). These results suggest that the effect of the different light
treatments on oil droplet pigmentation is progressive and occurs over several
weeks. There was no significant effect of light treatment on body mass
(two-sample t-test; juvenile t=-1.88, d.f.=8,
P=0.097; adult t=-0.75, d.f.=6, P=0.480) or of body
mass on oil droplet cut in either juvenile or adult
chickens (GLM: juvenile - C-type F1,7=0.04,
P=0.841; Y-type F1,7=0.24, P=0.640;
R-type F1,7=0.31, P=0.593; P-type
F1,7=0.70, P=0.430; adult - C-type
F1,5=0.22, P=0.661; Y-type
F1,5=4.87, P=0.078; R-type
F1,5=0.03, P=0.875; P-type
F1,5=0.34, P=0.585).
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With regard to retinal location, the mean cut values of
C- and P-type oil droplets in the ventral retina of adult chickens were
shifted significantly towards longer wavelengths compared with those in the
dorsal retina in both light-treatment groups (Tables
1,
4; Figs
2,
3). This was particularly
obvious in the P-type oil droplets, in which the increased contribution of a
secondary absorption peak at approximately 485 nm increased the absorption of
short-medium wavelengths in ventrally located cones
(Fig. 2); in the case of the
bright-light group, the absorptance spectrum of the ventral P-type oil droplet
in the double cones closely resembles that of the Y-type oil droplet in the
MWS single cones. Conversely, R-type oil droplets in the dorsal retina of both
adult and juvenile chickens were more densely pigmented and had mean
cut values shifted significantly towards longer wavelengths
than those in the ventral retina (Tables
2,
3 and
4; Figs
2,
3).
There was a significant effect of light treatment on the diameters of the C- and P-type oil droplets in the juvenile chickens (Table 3) and of the C-type oil droplets in the adult chickens (Table 4), and in each case the diameter of the oil droplets was larger in the dim-light group than in the bright-light group (Table 2). Moreover, the diameter of the C-type oil droplets in the juvenile chickens, and the C- and R-type oil droplets in the adults, was significantly larger in the dorsal retina than the ventral retina.
Effects on spectral sensitivity
The absorptance spectra of all pigmented oil droplet types from adult
chickens reared in dim light had cut values at shorter
wavelengths, and were therefore less densely pigmented than the corresponding
oil droplet types in the adult chickens reared in bright light. These
differences in spectral absorptance characteristics markedly affected the
modelled spectral sensitivity of the corresponding cone photoreceptor outer
segments (Fig. 4). In the case
of the MWS and LWS single cones, the reduction in pigmentation of the Y- and
R-type oil droplets in the chickens reared in dim light resulted in the
wavelength of peak sensitivity of their outer segments being shifted towards
shorter wavelengths, from 535 to 526 nm and from 600 to 585 nm, respectively,
and increased the overall sensitivity of the outer segments, by 52% and 58%,
respectively, compared with those in the chickens reared in bright light.
The effects of the dim-light treatment on the spectral sensitivities of the outer segments of SWS single cones containing a C-type oil droplet and of the LWS principal members of the double cones containing a P-type oil droplet were smaller in terms of spectral shift (475 to 472 nm and 573 to 572 nm, respectively) compared with the MWS and LWS single cones but were substantial in terms of overall sensitivity (increases of 11% and 18%, respectively). If the significant difference in C-type oil droplet diameter between bright- and dim-light-treatment groups (see above) is taken into consideration, the increase in spectral sensitivity of the SWS cones in the dim-light group would be considerably greater (62% more than SWS cones in the bright-light group).
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).
Although the absorptance spectra and cut values of the
oil droplets of the red jungle fowl (Gallus gallus), from which the
domestic chicken is derived (Fumihito et
al., 1994), are unknown, those of the chickens reared in bright
light are most similar to those of other wild-caught, wild-type diurnal bird
species (e.g. Hart et al.,
1998) and may well represent the `natural' condition for the
chicken. Moreover, the absorptance spectra of oil droplets in chickens reared
in dim light resemble those of carotenoid-deprived quails (Coturnix
coturnix japonica), the oil droplets of which are much less densely
pigmented than those of quail fed a carotenoid-rich `natural' diet
(Bowmaker et al., 1993). Light
intensities measured in rainforest habitats similar to those of the jungle
fowl vary from approximately 50-1000 lx in the shade to 10 000-18 000 lx in
areas illuminated via small gaps in the canopy
(Endler, 1993) (J. A. Endler,
personal communication). These values are similar to the illuminance levels
that would have been experienced by the bright-light-treatment group in the
present study.
Presumably, the chickens reared in dim light accumulated or maintained less
carotenoid pigment in the oil droplets to compensate for the reduced levels of
light available for vision. A reduction in pigmentation would allow more of
the incident photons to pass through the oil droplet and be absorbed by the
visual pigment within the outer segment. On the basis of electroretinographic
measurements of the spectral sensitivity of the SWS single cone in the pigeon,
Wortel and Nuboer calculated that less than 10% of the light reaching the
outer segment bypasses the oil droplet
(Wortel and Nuboer, 1986).
Consequently, while scattered light and any wave-guiding behaviour of oil
droplets might reduce slightly the effects of a decrease in oil droplet
pigmentation (or an increase in oil droplet diameter), the predicted increases
in spectral sensitivity of the cone outer segments in the chickens reared in
dim light are likely to be significant for enhancing visual sensitivity.
The modulation of oil droplet pigment density in response to changing light
intensity is perhaps analogous and/or additional to the adaptive anatomical
and physiological changes observed in the photoreceptors of other vertebrate
groups. For example, Penn and Williams showed that the rod photoreceptors of
laboratory rats raised in dim light (3 lx) had longer outer segments and a
higher density of visual pigment molecules than those raised under brighter
light (400 lx) and that the number of photons absorbed by the retina over time
was approximately constant regardless of incident light levels, a process they
called photostasis (Penn and Williams,
1986). Similarly, the outer segments of double cone photoreceptors
in the retina of the blue acara (Aequidens pulcher) are significantly
longer in animals raised in dim (<1 lx) `white' light than those raised in
bright (33-700 lx) `white' light
(Kröger et al.,
1999).
Changes in oil droplet pigmentation at the rate observed in the present
study (i.e. over the course of several weeks) might be adaptive for optimising
visual performance under the varying environmental conditions experienced by a
bird throughout its life, such as those arising from seasonal variations in
ambient light intensity or a shift between habitats during development or
migration. Similar intra-specific changes in spectral filtering have been
observed in mantis shrimps living in either deep- or shallow-water habitats,
in which both the intensity and spectral distribution of the ambient light
differ markedly (Cronin et al.,
2001; Cronin and Caldwell,
2002). Alternatively, the modulation of oil droplet pigmentation
might represent another form of retinal photostasis that regulates photon
capture across the retina, perhaps in response to local differences in
intensity caused by the physiological optics of the eye
(Penn and Williams, 1986). The
phenomenon of photostasis might also explain some of the intra-individual
variations in oil droplet cut between dorsal and ventral
retinal locations. In particular, the P-type oil droplets of double cones
located in the ventral retina are more densely pigmented than those located in
the dorsal retina. The ventral retina (which views the sky) will receive more
light, especially of shorter wavelengths
(Fig. 1), than the dorsal
retina (which views the ground), and the extra filtering of wavelengths below
500 nm might compensate for these intensity differences.
An alternative role for the increase in oil droplet carotenoid pigment
density in chickens reared in bright light compared with those reared in dim
light might be in the reduction of photo-oxidative damage in the retina.
Carotenoids are capable of quenching reactive oxygen species and organic free
radicals, such as those created as a result of intense irradiation of
biological tissue (Kirschfeld,
1982; Miki, 1991).
They might also reduce photo-oxidative damage indirectly by blocking the
transmission of high-energy UV radiation to the outer segment. However, the
variation in oil droplet colouration with cone type, the predictable
relationship between oil droplet cut and visual pigment
max in some cone types across species
(Hart and Vorobyev, 2005) and
the position of the oil droplet in the photoreceptor imply a significant role
in visual function. Moreover, it is not readily apparent how carotenoids
sequestered within the oil droplet would be able to quench photo-excited
molecules throughout the photoreceptor, let alone the rest of the retina,
through which the light has already passed before reaching the oil
droplets.
Carotenoids are mobilised from the skin, liver and fat reserves of birds
exposed to oxidative stress (Costantini
and Dell'omo, 2006) or in response to activation of the immune
system (Faivre et al., 2003).
Whether carotenoids are mobilised from the retinal cone oil droplets in
response to such physiological insults, and if so whether this might affect
visual sensitivity, is unknown, but it is a possibility that should be
considered when studying the effects of stress on visually guided behaviours,
such as mate choice.
Variations in the intensity and photoperiod of the ambient light
experienced during development are known to have other effects on the visual
system. For example, constant darkness (1 lx) or continuous light causes
enlargement of the eye and a reduction in corneal curvature in both turkeys
(Ashton et al., 1973;
Siopes et al., 1984;
Davis et al., 1986) and
chickens (Jenkins et al.,
1979; Oishi and Murakami,
1985; Li et al.,
2000; Liu et al.,
2004) that results in hyperopia. Such effects on the developing
avian eye have received considerable attention, partly because of the use of
the chicken as a model for growth-related ocular diseases in humans, but also
because of the importance of lighting conditions in poultry farming. Light
levels in the cages of intensively farmed chickens and turkeys might be as low
as 1 lx, either to save fuel costs, improve feed-conversion efficiency by
discouraging activity or reduce injurious pecking
(Manser, 1996;
Moinard and Sherwin, 1999;
Prescott and Wathes, 1999). It
is obvious from the foregoing that birds reared under such low light
conditions will exhibit morphological changes in their eyes that might be
detrimental to their welfare, and alternatives such as environmental
enrichment should be encouraged [e.g. as proposed by Sherwin et al.
(Sherwin et al., 1999)]. These
issues also highlight the need to maintain animals in conditions that are as
close to their natural habitat as possible prior to conducting any spectral or
anatomical studies of the retina.
Yew et al. reared chickens under different coloured lights and showed that
those raised under blue light had a higher proportion of R-type (LWS single
cone) oil droplets than those raised under white, red or yellow light
(Yew et al., 1978). However,
both wavelength discrimination ability and threshold spectral sensitivity in
chickens and pigeons are reportedly unaffected by early spectral deprivation
(Rudolph and Honig, 1972;
Brenner et al., 1983),
suggesting that any variations in visual performance due to changes in cone
proportions are compensated for at higher stages of the visual system.
Nevertheless, there is evidence from electrophysiological studies that
differences in oil droplet absorptance spectra might affect the spectral
sensitivity of the visual system, which suggests that the changes in oil
droplet pigmentation and cut observed in the present study
could have significant effects on vision. Brenner et al. showed that the
dorso-temporal retina or `red field' of the pigeon has a peak spectral
sensitivity at longer wavelengths than the ventro-nasal retina or `yellow
field' (Brenner et al., 1983).
Both the Y- and R-type oil droplets of the MWS and LWS single cones,
respectively, in the red field of the pigeon retina are more densely pigmented
and have cut values at longer wavelengths than those same
cone types in the yellow field (Bowmaker,
1977). Together with a higher proportion of MWS and LWS single
cones in the red field compared with the rest of the retina [(Waelchli, 1883),
cited in Bowmaker (Bowmaker,
1979)], these differences in oil droplet spectra might account for
the observed differences in spectral sensitivity. Similarly, the dorsal retina
of the chicken has a higher sensitivity to wavelengths between approximately
350 and 450 nm than the ventral retina
(Wortel et al., 1987). This
difference in relative sensitivity at short wavelengths might be because of
the reduced filtering of UV radiation by the P-type oil droplets in the dorsal
retina compared with those in the ventral retina
(Fig. 2).
Short-term, phenotypic changes in ocular anatomy or physiology, such as the
density of oil droplet pigmentation, reflect not only the susceptibility of
visual systems to altered lighting conditions, but also their functional
plasticity. Using a noise-limited model of spectral thresholds, Vorobyev
showed that the benefit to colour discrimination of pigmented oil droplets in
the avian retina was dependent on the intensity of the ambient light
(Vorobyev, 2003). Spectral
tuning by pigmented oil droplets allowed birds to discriminate more colours in
bright light. However, the reduction in photon capture caused by the pigmented
oil droplets, and the accompanying decrease in signal-to-noise ratio of the
cone responses, meant that the benefit of coloured oil droplets to vision was
marginal at light levels approximating those around twilight (
1-10 lx).
The reduction in levels of oil droplet pigmentation in chickens reared in dim
light in the present study suggests that absolute sensitivity is maintained at
the expense of spectral tuning (colour vision) under these conditions.
Speculating further, it is possible that, over evolutionary time, this would
create a selection pressure of sufficient strength to cause the reduction or
loss of oil droplet colouration in animals, including birds, that become more
nocturnal in habit. Indeed, the adoption of nocturnality has been proposed as
the reason for the loss of pigmentation in the cone oil droplets of marsupial
(metatherian) mammals and the loss of oil droplets altogether in placental
(eutherian) mammals (Walls,
1942).
In conclusion, although the cellular mechanisms responsible for modulating oil droplet pigment density are unknown, and are clearly a subject for further investigation, it is evident that the eyes of both vertebrates and invertebrates have several short- and long-term mechanisms to adapt to variations in the intensity and/or spectral distribution of the ambient illumination. Moreover, it is possible that many of these photostatic mechanisms offer a means for adaptive changes in visual system design over an evolutionary timescale.
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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