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Light intensity measurements, results from statistical analyses, and contrast estimates from a bird nest

Studies on animal colour vision typically focus on the chromatic aspect of colour, which is related to the spectral distribution, and disregard the achromatic aspect, which is related to the intensity (“brightness”) of a stimulus. Although the chromatic component of vision is often most reliable for object recognition because it is fairly context independent, the achromatic component may provide a reliable signal under specific conditions, for example at night when light intensity is low. Here we make a case for the importance of achromatic cues in plant-pollinator signalling, based on experimental data on naïve Deilephila elpenor and Macroglossum stellatarum hawkmoths, optical modelling and synthesising published experiments on bees, flies, butterflies and moths. Our experiments show that in ecologically relevant light levels hawkmoths express a strong preference for brighter stimuli. Published experiments suggest that for flower-visiting bees, butterflies, moths and flies, achromatic cues may be more important for object detection than often considered. Our optical modelling enabled disentangling the contribution of pigments and scattering structures to the flower’s achromatic contrast, and illustrates how flower anatomy and background are important mediating factors. We discuss our findings in the context of the often-assumed dichotomy between detection and discrimination, chromatic versus achromatic vision, and the evolution of floral visual signals.

Supplementary Methods and Figures

Most vertebrates have UV-sensitive vision, but the UV sensitivity of their eyes is limited by the transmittance of the ocular media, and the specific contribution of the different media (cornea, lens) has remained unclear. Here, we describe the transmittance of all ocular media (OMT), as well as that of lenses and corneas of birds. For 66 species belonging to 18 orders, the wavelength at which 50% of light is transmitted through the ocular media to the retina (λT0.5) ranges from 310 to 398 nm. Low λT0.5 corresponds to more UV light transmitted. Corneal λT0.5 varies only between 300 and 345 nm, whereas lens λT0.5 values are more variable (between 315 and 400 nm) and tend to be the limiting factor, determining OMT in the majority of species. OMT λT0.5 is positively correlated with eye size, but λT0.5 of corneas and lenses are not correlated with their thickness when controlled for phylogeny. Corneal and lens transmittances do not differ between birds with UV- and violet-sensitive SWS1 opsin when controlling for eye size and phylogeny. Phylogenetic relatedness is a strong predictor of OMT, and ancestral state reconstructions suggest that from ancestral intermediate OMT, highly UV-transparent ocular media (low λT0.5) evolved at least five times in our sample of birds. Some birds have evolved in the opposite direction towards a more UV-opaque lens, possibly owing to pigmentation, likely to mitigate UV damage or reduce chromatic aberration., Summary: UV sensitivity in bird eyes is determined by the transmittances of the cornea and lens. Pigmentation could explain some of the variation. Phylogenetically related birds are likely to have similar transmittance.

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.

Details about samples, validation of methods and additional transmittance curves

Figures S1-S7, Supplementary Table T1

Supplementary Figures S1-S4 and Extended Materials and Methods

S1. Experimental setup showing the white-UV (left) and green (right) backgrounds with the white-UV and blue feeders.

Animals are thought to use achromatic signals to detect small (or distant) objects and chromatic signals for large (or nearby) objects. While the spatial resolution of the achromatic channel has been widely studied, the spatial resolution of the chromatic channel has rarely been estimated. Using an operant conditioning method, we determined (i) the achromatic contrast sensitivity function and (ii) the spatial resolution of the chromatic channel of a diurnal raptor, the Harris's hawk Parabuteo unicinctus. The maximal spatial resolution for achromatic gratings was 62.3 c deg−1, but the contrast sensitivity was relatively low (10.8–12.7). The spatial resolution for isoluminant red-green gratings was 21.6 c deg−1—lower than that of the achromatic channel, but the highest found in the animal kingdom to date. Our study reveals that Harris's hawks have high spatial resolving power for both achromatic and chromatic vision, suggesting the importance of colour vision for foraging. By contrast, similar to other bird species, Harris's hawks have low contrast sensitivity possibly suggesting a trade-off with chromatic sensitivity. The result is interesting in the light of the recent finding that double cones—thought to mediate high-resolution vision in birds—are absent in the central fovea of raptors.

The presence of two spectrally different kinds of rod photoreceptors in amphibians has been hypothesized to enable purely rod-based colour vision at very low light levels. The hypothesis has never been properly tested, so we performed three behavioural experiments at different light intensities with toads (Bufo) and frogs (Rana) to determine the thresholds for colour discrimination. The thresholds of toads were different in mate choice and prey-catching tasks, suggesting that the differential sensitivities of different spectral cone types as well as task-specific factors set limits for the use of colour in these behavioural contexts. In neither task was there any indication of rod-based colour discrimination. By contrast, frogs performing phototactic jumping were able to distinguish blue from green light down to the absolute visual threshold, where vision relies only on rod signals. The remarkable sensitivity of this mechanism comparing signals from the two spectrally different rod types approaches theoretical limits set by photon fluctuations and intrinsic noise. Together, the results indicate that different pathways are involved in processing colour cues depending on the ecological relevance of this information for each task.This article is part of the themed issue ‘Vision in dim light’.

Vision is the primary sensory modality of birds, and its importance is evident in the sophistication of their visual systems. Coloured oil droplets in the cone photoreceptors represent an adaptation in the avian retina, acting as long-pass colour filters. However, we currently lack understanding of how the optical properties and morphology of component structures (e.g. oil droplet, mitochondrial ellipsoid and outer segment) of the cone photoreceptor influence the transmission of light into the outer segment and the ultimate effect they have on receptor sensitivity. In this study, we use data from microspectrophotometry, digital holographic microscopy and electron microscopy to inform electromagnetic models of avian cone photoreceptors to quantitatively investigate the integrated optical function of the cell. We find that pigmented oil droplets primarily function as spectral filters, not light collection devices, although the mitochondrial ellipsoid improves optical coupling between the inner segment and oil droplet. In contrast, unpigmented droplets found in violet-sensitive cones double sensitivity at its peak relative to other cone types. Oil droplets and ellipsoids both narrow the angular sensitivity of single cone photoreceptors, but not as strongly as those in human cones.