Ultraviolet colour perception in European starlings and Japanese quail
Ecology of Vision Laboratory, School of Biological Sciences, University of Bristol, Bristol, BS8 1UG, UK
* Author for correspondence (e-mail: Emma.Smith{at}bristol.ac.uk
Accepted 8 July 2002
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Summary |
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Key words: ultraviolet, UV, colour perception, European starling, Japanese quail, bird, vision, avian
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Introduction |
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Human vs avian colour vision
Humans have three different types of single cone photoreceptor. Each
contains a different photopigment that is either short (SWS), medium (MWS) or
long wavelength sensitive (LWS). For humans possessing normal colour vision,
three primary colours are required to match any colour and, thus, humans are
said to be trichromatic (Wyszecki and
Stiles, 1982). In contrast, most birds studied have four spectral
types of single cone (Bowmaker et al.,
1997
; Cuthill et al.,
2000
; Hart, 2001
),
so it is possible that they require four primary colours and hence are
tetrachromatic (Burkhardt,
1989
; Palacios et al.,
1990
; Palacios and Varela,
1992
; Bennett et al.,
1994
; Vorobyev et al.,
1998
; Osorio et al.,
1999
; Cuthill et al.,
2000
). Like humans, birds have SWS, MWS and LWS single cones,
although the cone photopigments of birds and primates are not homologous
(Yokoyama and Yokoyama, 1996
;
Wilkie et al., 1998
). Birds
also have either a cone with peak sensitivity in violet wavelengths and
considerable sensitivity in the near-ultraviolet (UVA, 320-400nm) region (VS
cone) or a cone with maximal sensitivity in the UVA region (UVS cone)
(Bowmaker et al., 1997
).
Possession of a VS cone appears to be typical of non-passerine birds such as
ducks and poultry (Wortel et al.,
1987
; Hart et al.,
1999
; Prescott and Wathes,
1999
), whereas possession of a UVS cone appears to be typical of
songbirds (oscine passerines; Hart et al.,
1998
; Bowmaker et al.,
1997
; Hart, 2001
)
and parrots (Bowmaker et al.,
1997
). Birds also have a substantial number of double cones across
their retina. The function of these cells is unclear, although they are not
thought to contribute to colour vision
(Maier and Bowmaker, 1993
;
Vorobyev et al., 1998
;
Cuthill et al., 2000
).
The presence of multiple photoreceptor types raises the question of how the
outputs of the receptors are neurally coded. If there are n cone
types, it is plausible that the animal has n-dimensional colour
vision. However, multiple pigments may instead only broaden the range of
wavelengths to which the animal is sensitive and may not be involved in
wavelength discrimination (D'Eath,
1998). Behavioural tests can distinguish between these
alternatives and establish the dimensionality of an animal's colour vision
(Jacobs, 1981
;
Goldsmith, 1990
;
Thompson et al., 1992
;
Varela et al., 1993
).
Birds have been shown to use UV cues in tasks such as foraging and mate
choice (e.g. Viitala et al.,
1995; Bennett et al.,
1996
; Andersson and Amundsen,
1997
; Bennett et al.,
1997
; Church et al.,
1998
; Johnson et al.,
1998
; Koivula and Viitala,
1999
; Sheldon et al.,
1999
; Maddocks et al.,
2002
; Siitari et al.,
2002
; Siitari and Viitala,
2002
). However, the way in which the output of the VS/UVS cone of
birds is neurally coded is not clear. If the VS/UVS cone output is purely used
in achromatic mechanisms, then surfaces that reflect more UV will appear
brighter to the bird. Alternatively, if the output of the VS/UVS cone is
utilised in chromatic vision, then birds could detect chromaticity differences
between surfaces according to their UV reflectivity relative to longer
wavelengths.
Three previous studies suggest that birds perceive UV as a chromatic rather
than an achromatic signal, but none is conclusive. The first study found that
songbirds could learn to discriminate between UV-reflective and
non-UV-reflective paint marks under natural light
(Derim-Oglu and Maximov,
1994). Discrimination performance was unaffected by small changes
in intensity of the stimuli, so it was concluded that the birds could perceive
UV chromaticity differences. However, UV reflectance in the stimuli was
created by mixing powdered chalk, which is highly UV reflective, with white
paint. This technique conceivably alters the surface properties of the paint
as well as its UV reflectance. As no controls were employed to ensure that the
birds really were using a UV cue, we cannot be sure whether the birds had
learnt a UV chromaticity or a texture discrimination.
The second piece of evidence comes from a series of matechoice studies
(Bennett et al., 1996;
Pearn et al., 2001
;
Maddocks et al., 2002
) in
which female birds preferred to associate with males viewed through
UV-transmitting rather than UV-blocking filters but did not show a preference
for males viewed under different levels of illumination. Although this
provides strong evidence that the birds were seeing and responding to UV
wavelengths, and not simply changes in intensity, it does not test directly
how UV cues are neurally processed.
The third study (Osorio et al.,
1999) provides compelling evidence that the four single cone
outputs of birds are compared for use in a colour vision system. Pairs of
domestic chicks learnt to discriminate between stimuli that were either UV
rich or UV poor under lighting conditions that excluded the use of the LWS or
MWS cones. However, although the stimuli were random in intensity, there were
no controls to check that the birds were really using UV as the discriminatory
cue for short wavelength discriminations. Also, we cannot be certain that
double cones were not involved in the discrimination, as Osorio et al.
(1999
) acknowledge.
Furthermore, the lighting conditions used in this experiment are unlikely to
be found in nature, and it is possible that a different pattern of results
would occur under lighting conditions more representative of natural light
environments. Indeed, Neumeyer and Arnold
(1989
) found that goldfish
only compare cone outputs under certain conditions. Goldfish shift from being
tetrachromatic at high light intensities to being trichromatic at lower light
intensities by dropping the LWS cone signal. Thus, even if we assume that the
chicks really were making a UV chromaticity discrimination under the
restricted lighting conditions of the Osorio et al.
(1999
) experiment, we still
cannot be sure how birds would normally see UV under full-spectrum light.
Natural light, which varies greatly in spectral irradiance, does contain UV
wavelengths, but the spectrum is dominated by longer wavelengths, particularly
under overcast conditions (Dixon,
1978
; Lythgoe,
1979
; Endler,
1990
). So, it is possible that under natural full-spectrum
lighting, the output of the UV cone is added to the output of the SWS cone to
increase the intensity detection at the short wavelength end of the spectrum.
What is clear, however, is that currently we do not know how the signal from
the VS/UVS cone is wired up.
To determine whether birds use their VS/UVS cone signal in a chromatic
mechanism, it is necessary to show behaviourally that they can distinguish the
UV part of the spectrum from other parts of the spectrum without using
intensity cues. It is not known exactly how the visual system of birds
produces the perception of brightness. However, it is possible to create
stimuli in which intensity is a totally unreliable cue and in which chromatic
signals are the only reliable predictive discriminatory cue (as in the study
by Osorio et al., 1999). The
ability to see UV chromatic signals can therefore be ascertained by giving the
bird a discrimination task in which it learns to discriminate between patterns
of random intensity that either do or do not contain UV reflectances. We used
such an associative learning technique to test the ability of European
starlings (Sturnus vulgaris) and Japanese quail (Coturnix
coturnix japonica) to make both short wavelength (UV vs
`non-UV') and long wavelength (orange vs red) discriminations under
full-spectrum lighting. The long-wavelength task was included as a positive
control, so that any failure on the UV discrimination could not be attributed
to some non-specific failure to learn the task. We chose to use starlings and
quail because they form models of the two main classes of avian colour vision
systems; starlings have a UVS cone typical of oscine passerine species and
quail have a VS cone typical of non-passerine species.
From an animal welfare perspective, if birds can see UV, the limited
emission of UV from artificial lights
(Lewis and Morris, 1998) may
be detrimental to captive birds, as it may limit the functional capacity of
their vision. There has already been some research in this area (e.g.
Moinard and Sherwin, 1999
;
Prescott and Wathes, 1999
;
Sherwin, 1999
;
Sherwin and Devereux, 1999
;
Jones et al., 2001
;
Moinard et al., 2001
;
Maddocks et al., 2001
).
However, the previous visual experience of an animal may affect its ability to
perceive UV, as many aspects of visual development rely on the animal being
exposed to a normal mixture of wavelengths during development. Although
Rudolph and Honig (1972
) found
that monochromatic rearing conditions did not affect the acquisition of
spectral discrimination in chicks, it is plausible that absence of UV
wavelength stimulation during rearing may lead to selective UV photoreceptor
damage and subsequent perceptual impairment. It is therefore possible that
supplementary UV may only benefit birds that have been reared under
UV-containing light. Consequently, we also compared the perceptual abilities
of quail that had been reared under UV-containing light (UV+) with quail that
had been reared under lighting that was deficient in UV (UV-).
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Materials and methods |
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Stimuli
Perceptual ability was tested by giving the birds a discrimination task in
which they were allowed to move freely around a foraging arena. In this arena,
there were always eight stimuli that overlay separate food wells (1.5
cmx1.0 cm diameter x depth). In every trial, four stimuli of one
colour were rewarded, and four stimuli of another were not rewarded with food.
If birds can perceive and remember the difference between the two sorts of
stimuli, then they should learn to ignore the unrewarded stimuli.
The stimuli were 2.5 cmx2.5 cm patterns consisting of a tiling of 121
grey squares of varying intensity (see Fig.
2 for examples). Birds are able to resolve at least four cycles
per degree (Schmid and Wildsoet,
1997), so the discrete squares should have been perceptible to the
animals. Each pattern was attached to the upper surface of a 37 g metal weight
of the same size as the pattern (Fig.
2) to increase the energetic cost of moving the stimuli and
thereby promote learning. On their lower surfaces, each weight was completely
coated with matt black paint. The sides and bottoms of all the weights were
laminated with Sellotape to prevent chipping of the paint, which may have
provided the birds with alternative cues with which to solve the task during
training. Birds were trained on three different visual discriminations, which
generated the three different experiments described below. In each experiment,
there were 12 pairs of training patterns.
|
Experiment 1
In experiment 1, the birds were trained to discriminate orange from red.
All squares in the patterns were set within a grey grid, the intensity of
which did not vary. Within each pattern, there were 35 randomly placed squares
that were either all red or all orange. Patterns were printed onto paper using
a colour inkjet printer (Epson Stylus Photo, 1440 d.p.i.). The patterns were
overlain by a 3 mm thick UV-blocking Perspex filter to prevent the birds
learning any discrimination based upon either UV reflection or UV-induced
fluorescence in longer wavelengths (see
Fig. 1 for transmission
spectrum, Fig. 2 for
photographs of stimuli and Fig.
3 for the reflectance of colours within them).
|
Experiment 2
In experiment 2, birds were trained to discriminate between UV-reflecting
and non-UV-reflecting patterns. In this experiment, we made both intensity and
chromatic cues available within the UV waveband to check that the birds could
perceive UV wavelengths. Different UV colours cannot be printed from a
standard inkjet printer, so the UV appearance of the patterns was manipulated
using filters. Grey waterproof insulating tape (Elephant tape, Sellotape GB
Ltd, Dunstable, UK), which is maximally reflective in the UV range, was used
to make a UV-reflective surface. Tilings of grey squares of random intensity,
similar to those used for experiment 1, were printed onto UV-transmitting
acetate and stuck down by their edges over this UV-reflecting surface.
Reflectance spectra (300-700 nm) taken with a Zeiss MCS 501 spectrophotometer
(Carl Zeiss Ltd, Oberkochen, Germany) showed that increasing the density of
grey squares printed onto acetate effectively reduced the reflected light
intensity of all wavelengths, including UV wavelengths. To manipulate UV
reflectance, these tilings of grey squares were subsequently overlain by
UV-transmitting or UV-blocking Perspex (transmission spectra are shown in
Fig. 1, a photograph of example
stimuli is shown in Fig. 2 and
the reflectance of the stimuli is shown in
Fig. 3). This manipulated the
chromaticity of all the squares within the pattern. To ensure that reliable
intensity cues were available within the UV waveband, we left some of the
squares in the overlying acetate pattern completely transparent and did not
alter the absolute intensity of the pattern grid surrounding the squares.
We tested that there was no obvious visible difference between the UV and non-UV patterns barring UV cues by showing 24 naive human observers (12 males and 12 females, age range 18-24 years) the stimuli for both experiment 1 and experiment 2 outdoors under natural light. The patterns chosen were identical in pattern and orientation but not in chromaticity and were presented in a two-alternative choice design. Observers were asked to classify the pairs of patterns as being the `same' or `different' and were blind to both the aims of the study and the nature of the differences between patterns. Humans naturally classify red and orange patterns as looking different (mean percent choices correct ± S.E.M. 97.9±1.53%), but performance at discriminating UV from non-UV patterns was random (mean percent choices correct ± S.E.M. 50.0±4.14%). The highly significant difference (t=10.87, d.f.=23, P<0.001) in human performance on the two tasks confirmed that there were no obvious alternative cues for the birds to learn in the UV task except differences within the UV waveband.
Experiment 3
In experiment 3, only chromatic cues were available to solve the task. None
of the squares within the pattern were left totally transparent, and the
absolute intensity of the individual squares within the pattern was highly
variable. The spatial layout of the pattern was always the same but there were
25 different levels of overall mean intensity. The intensity of our patterns
was manipulated by increasing or decreasing the density of ink printed on the
overlying acetate as appropriate. Measurements with a Zeiss MCS 501
spectrophotometer confirmed that increasing ink density effectively decreased
reflected light intensity in a linear manner and that our manipulation of
intensity was effective. We also attempted to manipulate the perceived
brightness of the squares within the patterns in an additional way by varying
the intensity of the grid around the squares. For humans, a dark grid makes
the squares within it appear less saturated than does a light grid. This
visual effect has never been demonstrated to apply in birds; however, even if
birds do not experience such induction effects, it was vital to ensure that
intensity of every aspect of the pattern was randomised. Consequently, no two
patterns had the same grid intensity, and grid intensity was randomised across
all the patterns.
Procedure
A bird was placed in a foraging arena, consisting of a cage containing a 60
cmx90 cm white Conti board on which there were eight equidistant food
wells. Because both quail and starlings are gregarious animals, a companion
animal was placed behind a wire partition on either side of the arena, so that
the test bird was never socially isolated at any time. The test birds did not
have access to food during the trials, apart from the food they obtained via
choosing stimuli. The apparatus was evenly illuminated by four wall-mounted
Durotest Truelite fluorescent lamps running on high-frequency (>30 kHz)
ballasts. During training, the ambient light was always UV+.
The birds were trained to push weights off the food wells in the arena using behavioural shaping techniques. They were subsequently trained to discriminate the stimuli for experiments 1, 2 and 3. Prior to training, each bird was deprived of food for 1-2 h to ensure that they were motivated to forage. On each trial, food was placed in four of the eight food wells on the board. The location of the rewarded food wells and the selection of training stimuli presented on each trial was randomised. For each bird, a certain colour was always placed over the food, and the other colour was always unrewarded. For long-wavelength discrimination experiments, half the animals were rewarded for choosing red rather than orange and vice versa; for short-wavelength discrimination experiments, half the animals were rewarded for choosing UV over non UV patterns and vice versa. While the arena was being set up for each trial, an opaque screen was placed between the birds and the experimenters so that the birds could not see where the food was being placed or the behaviour of the experimenters while they set up the board.
In each trial, birds were considered to have made a choice when they uncovered the food well by pushing off the patterned weight. The order of food wells visited by the bird in each trial was recorded in real-time on a laptop computer using Etholog (E. B. Ottoni, Sao Paulo, Brazil). Trials lasted one minute for the quails and 30 s for the starlings, which move much faster.
Birds were given up to 40 trials per day, with trials presented in blocks of 10. Within each block, trials were separated by approximately four minutes. Birds were rested for an hour between each block of trials to ensure that they stayed motivated. Training continued until the birds were performing well above chance. The learning performance of quail was assessed by scoring the proportion of choices correct out of the total choices per trial. Starlings never stopped uncovering all the food wells, regardless of whether they contained food or not, so instead they were assessed by scoring the proportion of choices correct out of the first four food wells they chose to visit. When a bird was at least 80% correct, averaged over its previous 10 training trials, it was considered to have learnt the discrimination to criterion.
A series of probe trials was given to ensure that the animals had learnt the desired discriminatory cue. The bird had to be 100% correct over two consecutive training trials to receive a probe trial. In probe trial 1, the bird was given a test in which there was no food in any of the food wells and in which all the stimuli were similar to those used in training but had not previously been seen by the bird. Correct performance showed that the birds were not using olfaction or simply recognising individual characteristics of the training stimuli. Probe trial 2 also used novel stimuli, but UV wavelengths were removed from the ambient light by placing a Lee 226 UV-blocking filter (see Fig. 1 for transmission spectra) over the lights in the room. This ascertained what effect removal of UV wavelengths had on performance. Probe trials 1 and 2 were repeated twice for each bird, using novel stimuli each time, and were carried out for all of the experiments. The order of probe trials given was counterbalanced over time. Each bird was given regular training trials in between probe trials to ensure that its performance was still at criterion, as learning could potentially be extinguished by the presentation of unrewarded trials.
For experiment 3, the birds were given a third probe trial to ascertain whether they were using chromatic or achromatic cues to make the discrimination. Although absolute intensity within the grid arrangement on each tile had been randomised in the training stimuli, this did not ensure that the birds did not see UV patterns as being brighter. If birds are more sensitive to the UV waveband than to the rest of the spectrum, then it is plausible that the UV patterns still looked brighter on average. In probe trial 3, UV patterns were three times darker than the non-UV patterns. Nevertheless, intensity within any individual pattern was highly variable, as before. Consequently, if a bird trained to choose UV patterns uses achromatic mechanisms to solve the task, then it will use the algorithm `always choose the brightest/lightest patterns'. In this case, a UV-trained bird should incorrectly select the much lighter non-UV patterns over the UV patterns. Conversely, if a bird trained to choose non-UV patterns uses achromatic mechanisms to solve the task, then it will use the algorithm `always choose the darkest patterns'. In this case, the non-UV trained birds should incorrectly select the much darker UV patterns. Performance on the first presentation of probe trial 3 was therefore critical, as the birds could potentially learn the obvious intensity difference between the UV and non-UV patterns over subsequent trials. Probe trial 3 was carried out three times per bird, interspersed by training trials and probe trials 1 and 2.
Analysis
For each experiment, the mean percentage of correct choices made was
calculated for the last 10 training trials prior to starting probe trials and
for the appropriate probe trials. For quail, the proportion of correct choices
was calculated from the total number of choices they made in a trial. For
starlings, the proportion correct out of their first four choices was
calculated. We compared the performance of the birds during their last 10
training trials with their performance on each type of probe trial using
one-sample t-tests.
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Results |
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Discussion |
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Tables 1, 2 and 3 show that the results for both species were very similar for experiments 1, 2 and 3. In all three experiments, both quail and starlings were over 80% correct during their last 10 training trials on each task. In probe trial 1, the birds always remained over 80% correct when novel stimuli were used without rewards. This confirms that (i) on each test the birds had learnt something general about the patterns rather than individual characteristics of the training stimuli and (ii) that they were not using olfaction. When UV wavelengths were removed from the ambient light (probe trial 2), performance remained high in experiment 1, indicating that removal of UV wavelengths does not alarm the birds sufficiently to prevent them from making discriminations (see Table 1). However, in experiments 2 and 3, performance dropped to random in probe trial 2, confirming that UV was the cue that the birds had been using to make the discriminations (see Tables 2, 3). In experiment 3, in which only chromatic signals were available as reliable cues, the performance of the bird on the task was resistant to large variations in the overall intensity of novel patterns, with birds still correctly selecting patterns of the appropriate wavelengths (see probe trial 3, Table 3). This further suggests that the birds were not making the discrimination between stimuli using achromatic cues but were instead using chromaticity differences.
Despite much evidence that birds see and use UV for ecologically relevant
tasks such as mate choice and foraging (reviewed in
Cuthill et al., 2000), there
has been relatively little investigation into the perceptual experience of UV.
Previous studies have strongly suggested that birds can discriminate spectral
stimuli, according to the signal of the UV cones relative to that in other
single cone types (Derim-Oglu and Maximov,
1994
; Bennett et al.,
1996
; Osorio et al.,
1999
), but all are open to alternative interpretations. The
experiments we describe here form a more watertight case that exemplars of
both poultry (Japanese quail) and passerines (European starlings) use UV
signals in a chromatic mechanism and can do so under full-spectrum
lighting.
The ability of these two species to make wavelength discriminations based upon the presence or absence of UV shows that the output of the VS/UVS cone is being compared with the output of one or more other cone types, not simply being added to it. Although this is not a demonstration of tetrachromacy, this experiment provides firm evidence that the VS/UVS cone is in some way opponently coded, and that birds have a dimension to their colour vision that humans do not. However, this experiment does not tell us with which other cone type, or types, the VS/UVS cone is being compared.
It is also still not known whether the VS/UVS cone contributes to the
perception of brightness as well as the perception of chromaticity
differences. It is well known that the SWS cone of humans contributes little,
if at all, to achromatic mechanisms
(Mollon, 1989), so it is
plausible that the VS/UVS cone of birds may, likewise, not be involved in
brightness perception. Current evidence suggests that this may be the case, as
avian perception of longer wavelengths appears to be involved in the detection
of both motion (Campenhausen and
Kirschfeld, 1998
) and visual texture
(Osorio et al., 2001
).
It has been suggested that supplemental UV lighting may benefit bird
welfare (e.g. Sherwin, 1999;
Sherwin and Devereux, 1999
;
Maddocks et al., 2001
;
Maddocks et al., 2002
).
However, if rearing birds without UV wavelengths selectively impairs their
ability to perceive it, birds that have been reared in UVconditions
will not be able to benefit from supplemental UV. As quail reared in UV
conditions could perceive UV wavelengths, rearing quail without UV wavelengths
does not seem to impair their ability to see and use UV cues. This is
consistent with previous work on birds showing that rearing under restricted
spectral distributions does not affect subsequent ability to make spectral
discriminations (Rudolph and Honig,
1972
). The two birds reared without UV appeared to learn the UV
discrimination as easily as their counterparts reared in UV+ conditions. With
such a small sample size, it is not possible to make a firm judgement as to
whether rearing without UV wavelengths affects the rate at which birds respond
to and learn about UV cues. However, it is possible that the visual rearing
environment affects later learned colour preferences and colour learning
(Miklósi et al., 2002
).
We could not test whether or not absence of UV during development prevents the
UVS cone of passerines from developing normally, as the starlings were wild
caught and had developed their visual systems under natural light. The VS cone
of quail would have been stimulated by blue light during development even in
the absence of UV and may be at lower risk of impairment through rearing in
the absence of UV compared with the UVS cones of passerines. As it is
currently thought that the provision of supplemental UV lighting may be
beneficial to bird welfare, this topic seems worthy of further
investigation.
In conclusion, both starlings and quail learnt colour differences in the UV waveband that are invisible to human observers, and the birds were clearly making choices based upon perceived wavelength differences in the stimuli. From these experiments, although we are now confident that the UV-sensitive cones of both passerines and poultry are involved in a colour opponency mechanism, we do not know with which cone types their output is compared nor the nature of the opponency. Further psychophysical and neurophysiological studies are needed to ascertain precisely how these particular photoreceptors work.
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Acknowledgments |
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References |
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Andersson, A. and Amundsen, T. (1997). Ultraviolet colour vision and ornamentation in bluethroats. Proc. R. Soc. Lond. B Biol. Sci. 264,1587 -1591.
Bennett, A. T. D., Cuthill, I. C. and Norris, K. J. (1994). Sexual selection and the mismeasure of color. Am. Nat. 144,848 -860.
Bennett, A. T. D., Cuthill, I. C., Partridge, J. C. and Maier, E. J. (1996). Ultraviolet vision and mate choice in zebra finches. Nature 380,433 -435.
Bennett, A. T. D., Cuthill, I. C., Partridge, J. C. and Lunau,
K. (1997). Ultraviolet plumage colors predict mate
preferences in starlings. Proc. Natl. Acad. Sci.
U.S.A. 94,8618
-8621.
Bowmaker, J. K., Heath, L. A., Wilkie, S. E. and Hunt, D. M. (1997). Visual pigments and oil droplets from six classes of photoreceptor in the retina of birds. Vision Res. 37,2183 -2194.[Medline]
Burkhardt, D. (1989). UV vision: a bird's eye view of feathers. J. Comp. Physiol. A 164,787 -796.
Campenhausen, M. v. and Kirschfeld, K. (1998). Spectral sensitivity of the accessory optic system of the pigeon. J. Comp. Physiol. A 183,1 -6.
Church, S. C., Bennett, A. T. D., Cuthill, I. C., Hunt, S., Hart, N. S. and Partridge, J. C. (1998). Does lepidopteran larval crypsis extend into the ultraviolet? Naturwissenschaften 85,189 -192.
Cuthill, I. C., Partridge, J. C., Bennett, A. T. D., Church, S. C., Hart, N. S. and Hunt, S. (2000). Ultraviolet vision in birds. Adv. Stud. Behav. 29,159 -214.
D'Eath, R. B. (1998). Can video images imitate real stimuli in animal behaviour experiments? Biol. Rev. 73,267 -292.
Derim-Oglu, E. N. and Maximov, V. V. (1994). Small passerines can discriminate ultraviolet surface colours. Vision Res. 34,1535 -1539.[Medline]
Dixon, E. R. (1978). Spectral distribution of Australian daylight. J. Opt. Soc. Am. 68,437 -450.
Endler, J. A. (1990). On the measurement and classification of colour in studies of animal colour patterns. Biol. J. Linnean Soc. 41,315 -352.
Goldsmith, T. H. (1990). Optimisation, constraint and history in the evolution of eyes. Q. Rev. Biol. 65,281 -322.[Medline]
Hart, N. S. (2001). The visual ecology of avian photoreceptors. Prog. Retin. Eye Res. 20,675 -703.[Medline]
Hart, N. S., Partridge, J. C. and Cuthill, I. C.
(1998). Visual pigments, oil droplets and cone photoreceptor
distribution in the European starling (Sturnus vulgaris).
J. Exp. Biol. 201,1433
-1446.
Hart, N. S., Partridge, J. C. and Cuthill, I. C. (1999). Visual pigments, cone oil droplets, ocular media & predicted spectral sensitivity in the domestic turkey (Meleagris gallopavo). Vision Res. 39,3321 -3328.[Medline]
Hunt, S., Cuthill, I. C., Bennett, A. T. D., Church, S. C. and
Partridge, J. C. (2001). Is the ultraviolet waveband a
special communication channel in avian mate choice? J. Exp.
Biol. 204,2499
-2507.
Jacobs, G. H. (1981). Comparative Colour Vision. London: Academic Press.
Jacobs, G. H. (1983). Colour-vision in animals. Endeavour 7,137 -140.[Medline]
Johnson, A., Andersson, S., Örnborg, J. and Lifjeld, J. T. (1998). Ultraviolet plumage ornamentation affects social mate choice and sperm competition in bluethroats (Aves: Luscinia s. svecica): a field experiment. Proc. R. Soc. Lond. B Biol. Sci. 265,1313 -1318.
Jones, E. K. M., Prescott, N. B., Cook, P., White, R. P. and Wathes, C. M. (2001). Ultraviolet light and mating behaviour in domestic broiler breeders. Br. Poult. Sci. 42, 23-32.[Medline]
Koivula, M. and Viitala, J. (1999). Rough-legged buzzards use vole scent marks to assess hunting areas. J. Avian Biol. 30,329 -332.
Lewis, P. D. and Morris, T. R. (1998). Responses of domestic poultry to various light sources. World Poult. Sci. J. 54,7 -25.
Lythgoe, J. N. (1979). The Ecology of Vision. Oxford: Oxford University Press.
Maddocks, S. A., Cuthill, I. C., Goldsmith, A. R. and Sherwin, C. M. (2001). Behavioural and physiological effects of absence of ultraviolet wavelengths for domestic chicks. Anim. Behav. 62,1013 -1019.
Maddocks, S. A., Bennett, A. T. D. and Cuthill, I. C. (2002). Rapid behavioural adjustments to unfavourable light conditions in European starlings (Sturnus vulgaris). Anim. Welfare 11,95 -191.
Maier, E. J. and Bowmaker, J. K. (1993). Colour vision in the passeriform bird, Leiothrix lutea: correlation of visual pigment absorbancy and oil droplet transmission with spectral sensitivity. J. Comp. Physiol. A 172,295 -301.
Miklósi, Á., Gonda, Z., Osorio, D. and Farzin, A. (2002). The effects of the visual environment on responses to colour by domestic chicks. J. Comp. Physiol. A 188,135 -140.
Moinard, C., Lewis, P. D., Perry, G. C. and Sherwin, C. M. (2001). The effects of light intensity and light source on injuries due to pecking of male domestic turkeys (Meleagris gallopavo). Anim. Welfare 10,131 -139.
Moinard, C. and Sherwin, C. M. (1999). Turkeys prefer fluorescent light with supplementary ultraviolet radiation. Appl. Anim. Behav. Sci. 64,261 -267.
Mollon, J. D. (1989). "Tho' she kneeled in the place where they grew...". The uses and origins of primate colour vision. J. Exp. Biol. 146, 21-38.[Abstract]
Neumeyer, C. and Arnold, K. (1989). Tetrachromatic color vision in the goldfish becomes trichromatic under white adaptation light of moderate intensity. Vision Res. 29,1719 -1727.[Medline]
Osorio, D., Miklósi, Á. and Gonda, Z. (2001). Visual ecology and perception of coloration patterns by domestic chicks. Evol. Ecol. 13,673 -689.
Osorio, D., Vorobyev, M. and Jones, C. D.
(1999). Colour vision of domestic chicks. J. Exp.
Biol. 202,2951
-2959.
Palacios, A., Martinoya, C., Bloch, S. and Varela, F. J. (1990). Color mixing in the pigeon a pyschophysical determination in the longwave spectral range. Vision Res. 30,587 -596.[Medline]
Palacios, A. G. and Varela, F. J. (1992). Color mixing in the pigeon (Columbia livia). 2. A psychophysical determination in the middle, short and near-UV wavelength range. Vision Res. 32,1947 -1953.[Medline]
Pearn, S. M., Bennett, A. T. D. and Cuthill, I. C. (2001). Ultraviolet vision, fluorescence and mate choice in a parrot, the budgerigar (Melopsittacus undulatus). Proc. R. Soc. Lond. B Biol. Sci. 268,2273 -2279.[Medline]
Prescott, N. B. and Wathes, C. (1999). Spectral sensitivity of the domestic fowl (Gallus g. domesticus). Br. Poult. Sci. 40,332 -339.[Medline]
Rudolph, R. L. and Honig, W. K. (1972). Effects of monochromatic rearing on spectral discrimination learning and the peak shift in chicks. J. Exp. Anal. Behav. 17,107 -111.[Medline]
Schmid, K. L. and Wildsoet, C. F. (1997). Contrast and spatial frequency requirements for emmetropization in chicks. Vision Res. 37,2011 -2021.[Medline]
Sheldon, B. C., Andersson, S., Griffith, S. C., Ornborg, J. and Sendecka, J. (1999). Ultraviolet colour variation influences blue tit sex ratios. Nature 402,874 -877.
Sherwin, C. M. (1999). Effects of environmental enrichment, fluorescent and intermittent lighting on injurious pecking amongst male turkey poults. Br. Poult. Sci. 40,592 -598.[Medline]
Sherwin, C. M. and Devereux, C. L. (1999). Preliminary investigations of ultraviolet-induced markings on domestic turkey chicks and a possible role in injurious pecking. Br. Poult. Sci. 40,429 -433.[Medline]
Siitari, H., Honkavaara, J., Huhta, E. and Viitala, J. (2002). Ultraviolet reflection and female mate choice in the pied flycatcher, Ficedula hypoleuca. Anim. Behav. 63, 97-102.
Siitari, H. and Viitala, J. (2002). Behavioural evidence for ultraviolet vision in a tetraonid species foraging experiment with black grouse Tetrao tetrix. J. Avian Biol. 33,199 -202.
Thompson, E., Palacios, A. and Varela, F. J. (1992). Ways of colouring: comparative colour vision as a case study for cognitive science. Behav. Brain Sci. 15, 1-74.
Varela, F. J., Palacios, A. G. and Goldsmith, T. H. (1993). Color vision in birds. In Vision, Brain and Behaviour in Birds (ed. H. P. Z. H. J. Bischoff), pp.77 -98. Massachusetts: MIT Press.
Viitala, J. E., Korpimaki, E., Palokangas, P. and Koivula, M. (1995). Attraction of kestrels to vole scent marks visible in ultraviolet light. Nature 373,425 -427.
Vorobyev, M., Osorio, D., Bennett, A. T. D., Marshall, N. J. and Cuthill, I. C. (1998). Tetrachromacy, oil droplets and bird plumage colours. J. Comp. Physiol. A 183,621 -633.[Medline]
Wilkie, S. E., Vissers, P. M. A. M., Das, D., DeGrip, W. J., Bowmaker, J. K. and Hunt, D. M. (1998). The molecular basis for UV vision in birds: spectral characteristics, cDNA sequence and retinal localisation of the UV-sensitive visual pigment of the budgerigar (Melopsittacus undulatus). Biochem. J. 330,541 -547.[Medline]
Wortel, J. F., Rugenbrink, H. and Nuboer, J. F. W. (1987). The photopic spectral sensitivity of the dorsal and ventral retinae of the chicken. J. Comp. Physiol. A 160,151 -154.
Wyszecki, G. and Stiles, W. S. (1982). Color Science, Concepts and Methods, Quantitative Data and Formulae. New York: John Wiley & Sons.
Yokoyama, S. and Yokoyama, R. (1996). Adaptive evolution of photoreceptors and visual pigments in vertebrates. Annu. Rev. Ecol. Syst. 27,543 -567.
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