Over a century ago workers such as J. Lubbock and K. von Frisch developed behavioural criteria for establishing that non-human animals see colour. Many animals in most phyla have since then been shown to have colour vision. Colour is used for specific behaviours, such as phototaxis and object recognition, while other behaviours such as motion detection are colour blind. Having established the existence of colour vision, research focussed on the question of how many spectral types of photoreceptors are involved. Recently, data on photoreceptor spectral sensitivities have been combined with behavioural experiments and physiological models to study systematically the next logical question: 'what neural interactions underlie colour vision?' This review gives an overview of the methods used to study animal colour vision, and discusses how quantitative modelling can suggest how photoreceptor signals are combined and compared to allow for the discrimination of biologically relevant stimuli.
Coloration mediates the relationship between an organism and its environment in important ways, including social signaling, antipredator defenses, parasitic exploitation, thermoregulation, and protection from ultraviolet light, microbes, and abrasion. Methodological breakthroughs are accelerating knowledge of the processes underlying both the production of animal coloration and its perception, experiments are advancing understanding of mechanism and function, and measurements of color collected noninvasively and at a global scale are opening windows to evolutionary dynamics more generally. Here we provide a roadmap of these advances and identify hitherto unrecognized challenges for this multi- and interdisciplinary field.
SUMMARY Recent studies have shown that certain nocturnal insect and vertebrate species have true color vision under nocturnal illumination. Thus, their vision is potentially affected by changes in the spectral quality of twilight and nocturnal illumination, due to the presence or absence of the moon,artificial light pollution and other factors. We investigated this in the following manner. First we measured the spectral irradiance (from 300 to 700 nm) during the day, sunset, twilight, full moon, new moon, and in the presence of high levels of light pollution. The spectra were then converted to both human-based chromaticities and to relative quantum catches for the nocturnal hawkmoth Deilephila elpenor, which has color vision. The reflectance spectra of various flowers and leaves and the red hindwings of D. elpenor were also converted to chromaticities and relative quantum catches. Finally, the achromatic and chromatic contrasts (with and without von Kries color constancy) of the flowers and hindwings against a leaf background were determined under the various lighting environments. The twilight and nocturnal illuminants were substantially different from each other, resulting in significantly different contrasts. The addition of von Kries color constancy significantly reduced the effect of changing illuminants on chromatic contrast, suggesting that, even in this light-limited environment,the ability of color vision to provide reliable signals under changing illuminants may offset the concurrent threefold decrease in sensitivity and spatial resolution. Given this, color vision may be more common in crepuscular and nocturnal species than previously considered.
Despite the scarcity of photons, Megalopta is able to visually orient to landmarks at night in a dark forest understory, an ability permitted by unusually sensitive apposition eyes and neural photon summation.
Humans are colour-blind at night, and it has been assumed that this is true of all animals. But colour vision is as useful for discriminating objects at night as it is during the day. Here we show, through behavioural experiments, that the nocturnal hawkmoth Deilephila elpenor uses colour vision to discriminate coloured stimuli at intensities corresponding to dim starlight (0.0001 cd x m(-2)). It can do this even if the illumination colour changes, thereby showing colour constancy-a property of true colour vision systems. In identical conditions humans are completely colour-blind. Our calculations show that the possession of three photoreceptor classes reduces the absolute sensitivity of the eye, which indicates that colour vision has a high ecological relevance in nocturnal moths. In addition, the photoreceptors of a single ommatidium absorb too few photons for reliable discrimination, indicating that spatial and/or temporal summation must occur for colour vision to be possible. Taken together, our results show that colour vision occurs at nocturnal intensities in a biologically relevant context.
Many animals use the spectral distribution of light to guide behaviour, but whether they have colour vision has been debated for over a century. Our strong subjective experience of colour and the fact that human vision is the paradigm for colour science inevitably raises the question of how we compare with other species. This article outlines four grades of 'colour vision' that can be related to the behavioural uses of spectral information, and perhaps to the underlying mechanisms. In the first, even without an (image-forming) eye, simple organisms can compare photoreceptor signals to locate a desired light environment. At the next grade, chromatic mechanisms along with spatial vision guide innate preferences for objects such as food or mates; this is sometimes described as wavelength-specific behaviour. Here, we compare the capabilities of di-and trichromatic vision, and ask why some animals have more than three spectral types of receptors. Behaviours guided by innate preferences are then distinguished from a grade that allows learning, in part because the ability to learn an arbitrary colour is evidence for a neural representation of colour. The fourth grade concerns colour appearance rather than colour difference: for instance, the distinction between hue and saturation, and colour categorization. These higher-level phenomena are essential to human colour perception but poorly known in animals, and we suggest how they can be studied. Finally, we observe that awareness of colour and colour qualia cannot be easily tested in animals.
Color vision is widespread among insects but varies among species, depending on the spectral sensitivities and interplay of the participating photoreceptors. The spectral sensitivity of a photoreceptor is principally determined by the absorption spectrum of the expressed visual pigment, but it can be modified by various optical and electrophysiological factors. For example, screening and filtering pigments, rhabdom waveguide properties, retinal structure, and neural processing all influence the perceived color signal. We review the diversity in compound eye structure, visual pigments, photoreceptor physiology, and visual ecology of insects. Based on an overview of the current information about the spectral sensitivities of insect photoreceptors, covering 221 species in 13 insect orders, we discuss the evolution of color vision and highlight present knowledge gaps and promising future research directions in the field. Expected final online publication date for the Annual Review of Entomology, Volume 66 is January 8, 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
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