Adrian G. Dyer

An Integrative Framework for the Appraisal of Coloration in Nature

The world in color presents a dazzling dimension of phenotypic variation. Biological interest in this variation has burgeoned, due to both increased means for quantifying spectral information and heightened appreciation for how animals view the world differently than humans. Effective study of color traits is challenged by how to best quantify visual perception in nonhuman species. This requires consideration of at least visual physiology but ultimately also the neural processes underlying perception. Our knowledge of color perception is founded largely on the principles gained from human psychophysics that have proven generalizable based on comparative studies in select animal models. Appreciation of these principles, their empirical foundation, and the reasonable limits to their applicability is crucial to reaching informed conclusions in color research. In this article, we seek a common intellectual basis for the study of color in nature. We first discuss the key perceptual principles, namely, retinal photoreception, sensory channels, opponent processing, color constancy, and receptor noise. We then draw on this basis to inform an analytical framework driven by the research question in relation to identifiable viewers and visual tasks of interest. Consideration of the limits to perceptual inference guides two primary decisions: first, whether a sensory-based approach is necessary and justified and, second, whether the visual task refers to perceptual distance or discriminability. We outline informed approaches in each situation and discuss key challenges for future progress, focusing particularly on how animals perceive color. Given that animal behavior serves as both the basic unit of psychophysics and the ultimate driver of color ecology/evolution, behavioral data are critical to reconciling knowledge across the schools of color research.

Honeybees (Apis mellifera) Learn Color Discriminations via Differential Conditioning Independent of Long Wavelength (Green) Photoreceptor Modulation

Background Recent studies on colour discrimination suggest that experience is an important factor in how a visual system processes spectral signals. In insects it has been shown that differential conditioning is important for processing fine colour discriminations. However, the visual system of many insects, including the honeybee, has a complex set of neural pathways, in which input from the long wavelength sensitive (‘green’) photoreceptor may be processed either as an independent achromatic signal or as part of a trichromatic opponent-colour system. Thus, a potential confound of colour learning in insects is the possibility that modulation of the ‘green’ photoreceptor could underlie observations. Methodology/Principal Findings We tested honeybee vision using light emitting diodes centered on 414 and 424 nm wavelengths, which limit activation to the short-wavelength-sensitive (‘UV’) and medium-wavelength-sensitive (‘blue’) photoreceptors. The absolute irradiance spectra of stimuli was measured and modelled at both receptor and colour processing levels, and stimuli were then presented to the bees in a Y-maze at a large visual angle (26°), to ensure chromatic processing. Sixteen bees were trained over 50 trials, using either appetitive differential conditioning (N = 8), or aversive-appetitive differential conditioning (N = 8). In both cases the bees slowly learned to discriminate between the target and distractor with significantly better accuracy than would be expected by chance. Control experiments confirmed that changing stimulus intensity in transfers tests does not significantly affect bee performance, and it was possible to replicate previous findings that bees do not learn similar colour stimuli with absolute conditioning. Conclusion Our data indicate that honeybee colour vision can be tuned to relatively small spectral differences, independent of ‘green’ photoreceptor contrast and brightness cues. We thus show that colour vision is at least partly experience dependent, and behavioural plasticity plays an important role in how bees exploit colour information.

Flower colour and phylogeny along an altitudinal gradient in the Himalayas of Nepal

Both the phylogenetic structure and trait composition of flowering plant communities may be expected to change with altitude. In particular, floral colours are thought to vary with altitude because Hymenoptera typically decline in importance as pollinators while Diptera and Lepidoptera become more important at higher elevations. Thus, ecological filtering among elevation zones and competitive processes among co-occurring species within zones could influence the floral chromatic cues present at low and high elevations. We collected data from 107 species of native flowering plants in the Himalaya Mountains of central Nepal over an elevation range of 900-4100 m, which includes habitat ranging from subtropical to subalpine within a relatively small geographical area. Using a phylogenetic framework, we asked whether and how flower colour diversity differed between species assemblages at lower and higher elevation, between monocots and eudicots, and between our sample from central Nepal and angiosperms from other regions of the world. There was significant phylogenetic clustering in the communities as a result of monocots, particularly orchids, which were found overwhelmingly at lower elevations. Phylogenetic signal for floral colours indicated that related species had colours that were more disparate than expected under Brownian motion evolution. Floral colours were significantly more diverse in the higher elevation subalpine zone than in the subtropical zone. However, the chromatic cues at both elevations were consistent with the hue discrimination abilities of the trichromatic hymenopteran visual system. Synthesis. Flower colour is not highly differentiated between subtropical and subalpine vegetation due to differences in the available orders of insect pollinators, or by the rate or direction of colour evolution in the lineages composing the two communities.

Blue colour preference in honeybees distracts visual attention for learning closed shapes

Spatial vision is an important cue for how honeybees (Apis mellifera) find flowers, and previous work has suggested that spatial learning in free-flying bees is exclusively mediated by achromatic input to the green photoreceptor channel. However, some data suggested that bees may be able to use alternative channels for shape processing, and recent work shows conditioning type and training length can significantly influence bee learning and cue use. We thus tested the honeybees’ ability to discriminate between two closed shapes considering either absolute or differential conditioning, and using eight stimuli differing in their spectral characteristics. Consistent with previous work, green contrast enabled reliable shape learning for both types of conditioning, but surprisingly, we found that bees trained with appetitive-aversive differential conditioning could additionally use colour and/or UV contrast to enable shape discrimination. Interestingly, we found that a high blue contrast initially interferes with bee shape learning, probably due to the bees innate preference for blue colours, but with increasing experience bees can learn a variety of spectral and/or colour cues to facilitate spatial learning. Thus, the relationship between bee pollinators and the spatial and spectral cues that they use to find rewarding flowers appears to be a more rich visual environment than previously thought.

Linearisation of RGB camera responses for quantitative image analysis of visible and UV photography: a comparison of two techniques.

Linear camera responses are required for recovering the total amount of incident irradiance, quantitative image analysis, spectral reconstruction from camera responses and characterisation of spectral sensitivity curves. Two commercially-available digital cameras equipped with Bayer filter arrays and sensitive to visible and near-UV radiation were characterised using biexponential and Bézier curves. Both methods successfully fitted the entire characteristic curve of the tested devices, allowing for an accurate recovery of linear camera responses, particularly those corresponding to the middle of the exposure range. Nevertheless the two methods differ in the nature of the required input parameters and the uncertainty associated with the recovered linear camera responses obtained at the extreme ends of the exposure range. Here we demonstrate the use of both methods for retrieving information about scene irradiance, describing and quantifying the uncertainty involved in the estimation of linear camera responses.

Evaluating the spectral discrimination capabilities of different pollinators and their effect on the evolution of flower colors

Important plant pollinators like bees and birds have very different color visual systems. Previous work has attempted to relate flower syndromes to the respective visual capabilities of the most important pollinators, but has often been limited by the lack of robust means to make between-species comparisons of how flower color signals are processed. In a recent study we solved this dilemma by comparing the raw spectral signals, quantifiable by major inflection points on a wavelength scale, from different flowers whose pollinators were known from direct observation. Here we elaborate on how this method allows robust cross species comparisons that are independent of the requirement to know the complex and often inaccessible physiological data about color processing in different animals. The use of this method should thus allow for the testing of pollinator syndrome hypotheses for different animal pollinators from different regions of the world.

Hymenopteran pollinators as agents of selection on flower colour in the New Zealand mountains: salient chromatic signals enhance flower discrimination

Abstract Flowering plants in New Zealand have often been described as having predominantly small white or pale flowers, possibly due to an absence of social insects as a major pollinating force. However, insect vision is considerably different to human perception, and these hypotheses need to be assessed considering insect perceptual capabilities. We collected spectral reflectance data from flowers of 23 native species in an alpine region of New Zealand at an altitude above 1500 m where 77% of flowers have been reported to possess small white or pale flowers. Our spectral analyses show that these flowers actually have very strong chromatic signals for hymenoptera colour vision. Indeed the spectral signals of these flowers most frequently have inflection points at about 400 and 500 nm, which closely match the region of best spectral discrimination by hymenopteran pollinators with a trichromatic visual system. When the flower spectra are plotted in a colour space designed for hymenoptera, the data reveals that most of the flower colours would be well detected against background foliage, and often reliably discriminated from the other flowers appearing in the same alpine environment. We thus demonstrate that New Zealand alpine flowers are actually well suited for visual detection and discrimination by biologically important hymenopteran pollinators.

Learning context modulates aversive taste strength in honey bees

ABSTRACT The capacity of honey bees (Apis mellifera) to detect bitter substances is controversial because they ingest without reluctance different kinds of bitter solutions in the laboratory, whereas free-flying bees avoid them in visual discrimination tasks. Here, we asked whether the gustatory perception of bees changes with the behavioral context so that tastes that are less effective as negative reinforcements in a given context become more effective in a different context. We trained bees to discriminate an odorant paired with 1 mol l−1 sucrose solution from another odorant paired with either distilled water, 3 mol l−1 NaCl or 60 mmol l−1 quinine. Training was either Pavlovian [olfactory conditioning of the proboscis extension reflex (PER) in harnessed bees], or mainly operant (olfactory conditioning of free-walking bees in a Y-maze). PER-trained and maze-trained bees were subsequently tested both in their original context and in the alternative context. Whereas PER-trained bees transferred their choice to the Y-maze situation, Y-maze-trained bees did not respond with a PER to odors when subsequently harnessed. In both conditioning protocols, NaCl and distilled water were the strongest and the weakest aversive reinforcement, respectively. A significant variation was found for quinine, which had an intermediate aversive effect in PER conditioning but a more powerful effect in the Y-maze, similar to that of NaCl. These results thus show that the aversive strength of quinine varies with the learning context, and reveal the plasticity of the bees gustatory system. We discuss the experimental constraints of both learning contexts and focus on stress as a key modulator of taste in the honey bee. Further explorations of bee taste are proposed to understand the physiology of taste modulation in bees. Summary: Learning context is a key modulator of taste in the honey bee.

Flower Colours through the Lens: Quantitative Measurement with Visible and Ultraviolet Digital Photography

Background The study of the signal-receiver relationship between flowering plants and pollinators requires a capacity to accurately map both the spectral and spatial components of a signal in relation to the perceptual abilities of potential pollinators. Spectrophotometers can typically recover high resolution spectral data, but the spatial component is difficult to record simultaneously. A technique allowing for an accurate measurement of the spatial component in addition to the spectral factor of the signal is highly desirable. Methodology/Principal findings Consumer-level digital cameras potentially provide access to both colour and spatial information, but they are constrained by their non-linear response. We present a robust methodology for recovering linear values from two different camera models: one sensitive to ultraviolet (UV) radiation and another to visible wavelengths. We test responses by imaging eight different plant species varying in shape, size and in the amount of energy reflected across the UV and visible regions of the spectrum, and compare the recovery of spectral data to spectrophotometer measurements. There is often a good agreement of spectral data, although when the pattern on a flower surface is complex a spectrophotometer may underestimate the variability of the signal as would be viewed by an animal visual system. Conclusion Digital imaging presents a significant new opportunity to reliably map flower colours to understand the complexity of these signals as perceived by potential pollinators. Compared to spectrophotometer measurements, digital images can better represent the spatio-chromatic signal variability that would likely be perceived by the visual system of an animal, and should expand the possibilities for data collection in complex, natural conditions. However, and in spite of its advantages, the accuracy of the spectral information recovered from camera responses is subject to variations in the uncertainty levels, with larger uncertainties associated with low radiance levels.

Trade-off between camouflage and sexual dimorphism revealed by UV digital imaging: the case of Australian Mallee dragons (Ctenophorus fordi)

SUMMARY Colour patterns displayed by animals may result from the balance of the opposing requirements of sexual selection through display and natural selection through camouflage. Currently, little is known about the possibility of the dual purpose of an animal colour pattern in the UV region of the spectrum, which is potentially perceivable by both predators and conspecifics for detection or communication purposes. Here, we implemented linearised digital UV photography to characterise and quantify the colour pattern of an endemic Australian Agamid lizard classically regarded as monomorphic when considering data from the visible region of the spectrum. Our results indicate a widespread presence of UV elements across the entire body of the lizards and these patterns vary significantly in intensity, size and frequency between sexes. These results were modelled considering either lizard or avian visual characteristics, revealing that UV reflectance represents a trade-off between the requirements of sexual displaying to conspecifics and concealment from avian predators.