10 July 2004

(51) BIRDS: Ultraviolet Vision

Exploring the Fourth Dimension

The vivid colours of many animals and plants are not only a source of
inspiration to artists and poets, but are of great interest to evolutionary
biologists. Ever since Darwin, biologists have used colour variation to test the
theory of natural selection itself, and more specific evolutionary theories of
signalling, crypsis, mimicry and warning coloration, to name but a few. But in
the last decade, the hottest area of research has been sexual selection,
Darwin's theory of how female mating preferences can lead to the elaboration of
colourful ornaments such as the peacock's tail. Indeed, birds have been the most
popular group for such research, but scientists in the Ecology of Vision group
at the School of Biological Sciences (University of Bristol) have argued that
much of this work is fundamentally flawed.


If you watched a wildlife series with, say, the red light source of your
television removed (or if you were red-green "colour-blind") and you then came
up with conclusions about colour variation in the natural world, would anyone
believe you? Probably not, but then that is what we humans are doing every time
we think we are seeing the colour world of non-human animals. Unlike other
variables such as length, width, mass, or time of day, colour is not an inherent
property of the object; it is a property of the nervous system of the animal
perceiving the light. In an interdisciplinary collaboration Andrew Bennett,
Innes Cuthill and Julian Partridge have been combining techniques from visual
physiology and behavioural ecology to investigate the colour world of birds.

Colour Vision in Humans

The sensation of colour stems from the differential stimulation of the different
types of photoreceptors in the retina. Each cone type produces an output, and it
is their differences in output at a particular point on the retina which
underlies the sensation of colour. In humans there are only three types of
cones, absorbing maximally in different regions of the spectrum. Due to the
appearance (to humans) of monochromatic light at these wavelengths, these three
cone types are called "red", "green" and "blue" respectively. Consequently, for
humans, all hues can be produced by mixing red, green and blue light. This is
how a colour television set works; a mixture of three wavelengths produces
several million apparent "colours". This mechanism has a number of consequences.
-(1) Different wavelength spectra can produce the same hue; as long as the output
from the three types of cone remains the same, the hue is the same.
-(2) The same wavelength spectra will produce different hues to animals that differ
in the absorption spectra of their cone types.
-(3) Humans have trichromatic, or three-dimensional, colour vision because we have
three interacting cone types.
Animals with two interacting cone types, such as most mammals other than
old-world primates, have two-dimensional colour vision (similar perhaps to the
faulty colour TV set mentioned earlier). It is harder to imagine what colour
vision with more dimensions than three might be like, but animals with 4 and
5-dimensional colour vision exist.

Colour Vision in Birds

Bird colour vision differs from that of humans in two main ways. First, birds
can see ultraviolet light. It appears that UV vision is a general property of
diurnal birds, having been found in over 35 species using a combination of
microspectrophotometry, electrophysiology, and behavioural methods. So, are
birds like bees? Bees, like humans, have three receptor types, although unlike
humans they are sensitive to ultraviolet light, with loss of sensitivity at the
red end of the spectrum. This spectral range is achieved by having a cone type
that is sensitive to UV wavelengths, and two that are sensitive to "human
visible" wavelengths. Remember, because 'colour' is the result of differences in
output of receptor types, this means that bees do not simply see additional 'UV
colours', they will perceive even human-visible spectra in different hues to
those which humans experience. Fortunately, as any nature film crew knows, we
can gain an insight to the bee colour world by converting the blue, red and
green channels of a video camera into UV, blue and green channels. Bees are
trichromatic, like humans, so the three dimensions of bee colour can be mapped
onto the three dimensions of human colour. With birds, and indeed many other
non-mammalian vertebrates, life is not so simple. As well as seeing very well in
the ultraviolet, all bird species that have been studied have at least four
types of cone. They have four, not three, dimensional colour vision. Recent
studies have confirmed tetra-chromacy in some fish and turtles, so perhaps we
should not be surprised about this. It is mammals, including humans, that have
poor colour vision! Whilst UV reception increases the range of wavelengths over
which birds can see, increased dimensionality produces a qualitative change in
the nature of colour perception that probably cannot be translated into human
experience. Bird colours are not simply refinements of the hues that humans, or
bees, see, these are hues unknown to any trichromat.

Investigating animal colours

Why have so many behavioural and evolutionary ecologists failed to recognise
that human colour perceptions are irrelevant for their studies? One reason is
the feeling, long dismissed by philosophers, that perception mirrors an
objective reality. Yet whilst reflectance spectra can be quantified independent
of the observer, colours cannot. Second, until relatively recently it was
thought that humans had amongst the best colour vision of any animal, and that
most animals' spectral sensitivities lay within the human-visible spectrum. This
misapprehension still persists outside the visual sciences. A corollary is that
we have long accepted that birds have (human-like) colour vision because many
birds are colourful to us. The notion that plumages may be even more colourful
to birds, or simply colourful in different ways, has not been widely considered,
even though we readily accept that a dog's sense of smell is far richer than our
own. The fact that human colour experience can only really be applied to other
old world primates has important consequences for testing evolutionary
hypotheses. Many of the objects to which evolutionary hypotheses apply, reflect
in the UV. Many fruit, flowers, and seeds contrast with their background much
more strongly in UV than human-visible wavelengths. Furthermore, and of
particular interest to research on sexual selection and mate choice, so do many
species of birds' plumage. For example, male and female blue tits look similar
to us, but there is a significant sex difference in the UV reflection of several
plumage regions (e.g. the 'blue' crest). Some 'human-white' feathers are
UV-reflecting, some are not. Reflectance spectroradiometry and multi-spectral
cameras that extend into the ultraviolet allow the Bristol team to quantify
plumage patterns objectively. By using selective filters to cut out particular
wavelengths of light, behavioural experiments have already shown that the
ultraviolet component of plumage colours is important in mate choice decisions
for species such as starlings and zebra finches. The Bristol approach is to link
behavioural ecology to a research program in colour cognition, for if we wish to
understand evolutionary hypotheses involving colour we need to understand how
animals perceive colour. Ultimately this will not only improve our understanding
of animal signals, but might give us an insight to the function and evolution of
the different colour vision systems that exist across the animal kingdom.

© University of Bristol 2004