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Fig. S1. Imaging scatterometry of the buttercup Ranunculus acris and the kingcup Caltha palustris. (a) Diagram of a reflecting and scattering buttercup petal. Incident light is partly specularly reflected (white arrows) and diffusely scattered and transmitted (yellow arrows). (b) Scatterogram of the smooth and flat adaxial side of a petal of R. acris, showing a local bright spot, indicating specular reflection, and a diffuse yellow scattering pattern. (c) Epiillumination of the lower epidermis of R. acris, showing the slightly rough surface. (d) Scatterogram of the abaxial side of a petal of R. acris, showing a very diffuse yellow pattern. (e) The upper epidermis of the kingcup Caltha palustris illuminated from a slightly oblique side, showing the cone-shaped epidermal cells. (f) Scatterogram of the upper epidermis of C. palustris demonstrating very diffuse scattering. Scale bar (c, e): 50 µm. The red circles in (a)  

Fig. S1. Imaging scatterometry of the buttercup Ranunculus acris and the kingcup Caltha palustris. (a) Diagram of a reflecting and scattering buttercup petal. Incident light is partly specularly reflected (white arrows) and diffusely scattered and transmitted (yellow arrows). (b) Scatterogram of the smooth and flat adaxial side of a petal of R. acris, showing a local bright spot, indicating specular reflection, and a diffuse yellow scattering pattern. (c) Epiillumination of the lower epidermis of R. acris, showing the slightly rough surface. (d) Scatterogram of the abaxial side of a petal of R. acris, showing a very diffuse yellow pattern. (e) The upper epidermis of the kingcup Caltha palustris illuminated from a slightly oblique side, showing the cone-shaped epidermal cells. (f) Scatterogram of the upper epidermis of C. palustris demonstrating very diffuse scattering. Scale bar (c, e): 50 µm. The red circles in (a)  

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Buttercup (Ranunculus spp.) flowers are exceptional because they feature a distinct gloss (mirror-like reflection) in addition to their matte-yellow coloration. We investigated the optical properties of yellow petals of several Ranunculus and related species using (micro)spectrophotometry and anatomical methods. The contribution of different petal...

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... Previous studies have shown that differences in floral color can induce pollinators to behave selectively toward certain flowers (Vickery, 1992;Schemske and Bradshaw, 1999;Hirota et al., 2012). Flower color involves two optical phenomena: (i) the reflection and scattering of light by floral structures, and (ii) wavelength-selective absorption by floral pigments (Kay et al., 1981;Lee, 2007;Vignolini et al., 2012;Stavenga and van der Kooi, 2016;van der Kooi et al., 2017;Wilts et al., 2018). Although much remains to be studied about the optical properties of flowers, we know that due to the different refractive indices of the petals' cellular components, incident light is reflected and scattered (Vignolini et al., 2012;Stavenga and van der Kooi, 2016;van der Kooi et al., 2017;Wilts et al., 2018). ...
... Flower color involves two optical phenomena: (i) the reflection and scattering of light by floral structures, and (ii) wavelength-selective absorption by floral pigments (Kay et al., 1981;Lee, 2007;Vignolini et al., 2012;Stavenga and van der Kooi, 2016;van der Kooi et al., 2017;Wilts et al., 2018). Although much remains to be studied about the optical properties of flowers, we know that due to the different refractive indices of the petals' cellular components, incident light is reflected and scattered (Vignolini et al., 2012;Stavenga and van der Kooi, 2016;van der Kooi et al., 2017;Wilts et al., 2018). Pigments, on the other hand, have been extensively characterized with respect to their spectral properties, biosynthesis and biological functions. ...
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The Atacama Desert, one of the driest places on earth, holds a rich biodiversity that becomes most appreciable in years when unusual rainfall accumulation triggers a phenomenon of explosive development of ephemeral herbaceous and woody desert species known as “desierto florido” or “blooming desert.” Despite the scientific importance of this unique phenomenon only few studies have addressed the mechanisms of flower phenotypic divergence under the fluctuating environment provided by this recurrent event. We investigated the mechanisms of floral color diversity in Cistanthe longiscapa (Montiaceae), a dominant species across the ephemeral blooming landscape of Atacama Desert. Our analyses show that the variation in colors of C. longiscapa flowers result from petals containing betalain pigments with different absorption spectra. The different pigment composition of petals causes flower color differences in the visible and ultraviolet (UV) range of the spectrum. Through color vision models we show that C. longiscapa flowers are highly polymorphic in their color appearance for insect pollinators. Our results highlight the variable nature in flower color of C. longiscapa varieties blooming simultaneously in a geographical restricted area. Given the importance of color in attracting floral visitors, the observed color variability could contribute to increased cross pollination in extreme desert conditions, while accounting for complex and fluctuating histories of plant-pollinator interactions.
... Pigment appearance can change according to their subcellular location and the shape of the cell. Cell shape and cuticle texture constitute tridimensional structures that impact the path of light entering or exiting the cell, modifying the visual aspect of the petal or even producing colours through light diffraction and constructive interference [4,[91][92][93][94][95][96][97]. Thus, colour patterns could, in theory, emerge not by modifying pigment production locally but by varying cell shape and texture across the petal surface ( Figure 1B). ...
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Colourful spots, stripes and rings decorate the corolla of most flowering plants and fulfil important biotic and abiotic functions. Spatial differences in the pigmentation of epidermal cells can create these patterns. The last few years have yielded new data that have started to illuminate the mechanisms controlling the function, formation and evolution of petal patterns. These advances have broad impacts beyond the immediate field as pigmentation patterns are wonderful systems to explore multiscale biological problems: from understanding how cells make decisions at the microscale to examining the roots of biodiversity at the macroscale. These new results also reveal there is more to petal patterning than meets the eye, opening up a brand new area of investigation. In this mini-review, we summarise our current knowledge on the Eco-Evo-Devo of petal pigmentation patterns and discuss some of the most exciting yet unanswered questions that represent avenues for future research.
... 3,4 In addition to cephalopods, there are other organisms that combine structural color with pigmental color: buttercup petals have both carotenoid pigments for yellowness and thin films for reflection. 5 The shape and color adaptions found in nature have inspired the fabrication of soft actuators with integrated color changes in the lab 6 as such materials can be adapted for use in soft robotics for signaling, camouflage, and temperature regulation. ...
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Cuttlefish can modify their body shape and both their pigmentary and structural colors for protection. This adaptability has inspired the development of appearance-changing polymers such as structural color actuators, although in most cases, the original shape has been confined to being flat, and pigmented structural color actuators have not yet been reported. Here, we have successfully created a pigmented structural color actuator using a cholesteric liquid crystal elastomer with a lower actuation temperature where both actuation and coloration (structural and pigmental) are tunable with temperature and NIR light. The shape, structural color, and absorption of the NIR-absorbing dye pigment of the actuator all change with temperature. Light can be used to trigger local in-plane bending actuation in flat films and local shape changes in a variety of 3D-shaped objects. A cuttlefish mimic that can sense light and respond by locally changing its appearance was also made to demonstrate the potential of pigmented structural color actuators for signaling and camouflage in soft robotics.
... The illumination spectrum (Figure 1A) was measured using a calibrated spectroradiometer (RSP900-R; International Light, Peabody, MA, United States). Reflectance spectra of stimuli and background ( Figure 1B) were measured using an integrating sphere and the same setup, following standard routines (van der Kooi et al., , 2017. The used reference was a diffuse, white tile (Avantes WS-2). ...
... A similar preference for the brighter of the two shades of the same colour has earlier been shown for M. stellatarum (Kelber, 2005); that study had been performed under higher illumination intensity (≈4,000 lux) and used (monochromatic) light sources with fairly high intensity differences as stimuli, whereas the stimuli used here are more similar to natural flowers. Although the peak reflectance of the Light Blue stimulus used here is still somewhat higher (80%) than the highest reflectance found in flowers (∼60%; van der Kooi et al., , 2017, the strong preference (Figures 1C,D) can likely be generalised to natural flowers. ...
... The optical model is based on the Kubelka-Munk theory for scattering and absorbing media and relies on spectral measurements as input. The model enables to systematically investigate the contribution of different optical properties, such as the amount of scattering or pigmentation (van der Kooi et al., , 2017van der Kooi and Stavenga, 2019). We used a white, blue, yellow and ultraviolet-reflecting red flower (Silene latifolia-alba, Nolana paradoxa, Oenothera macrocarpa, and Papaver rhoeas, respectively), systematically varied their scattering coefficient independent from pigmentation properties and calculated the achromatic contrast against a green leaf or blue-sky background (D65, midday). ...
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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.
... The mesophyll can also influence the appearance of petals by reflecting or diffusing light. For example, buttercup petals (yellow-colored Ranunculus) have a reflective starch-containing parenchyma cell layer just underneath their epidermis, participating to the glossy and reflective petal surface (Parkin, 1928(Parkin, , 1931Vignolini et al., 2012;van der Kooi et al., 2017). By a similar mechanism, the mesophyll of poppies and kingcup (Caltha palustris) petals contains large air cavities, creating a difference in refractive indices of the petal tissues and therefore strong light reflection and scattering, participating to the shiny appearance of the petals (Whatley, 1984;van der Kooi and Stavenga, 2019). ...
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Petals are typified by their conical epidermal cells that play a predominant role for the attraction and interaction with pollinators. However, cell identities in the petal can be very diverse, with different cell types in subdomains of the petal, in different cell layers, and depending on their adaxial-abaxial or proximo-distal position in the petal. In this mini-review, we give an overview of the main cell types that can be found in the petal and describe some of their functions. We review what is known about the genetic basis for the establishment of these cellular identities and their possible relation with petal identity and polarity specifiers expressed earlier during petal development, in an attempt to bridge the gap between organ identity and cell identity in the petal.
... In recent years there has been rapid growth in the appreciation that surface structure of plant flower petals may produce a variety of optical effects that may contribute to the colour perception of bee pollinators. Proposed optical structures include iridescence (Glover & Whitney 1999;Vignolini et al. 2015), specular reflections (gloss) (Galsterer et al 1999;Vignolini et al. 2012;Whitney et al. 2012;van der Kooi et al. 2017), and "halos" (Moyroud et al. 2017), although how such optical effects may fit a formal definition for flower colour signalling has only been tested in relatively few behavioural studies (Whitney et al. 2016;Dyer et al. 2007;Garcia et al. 2019; see van der Kooi et al. 2019 for review). For example, structural colours such as iridescence have been proposed to be important signals that may be present in flowering plant species, since it has been shown that free flying bumblebees can learn such information with appetitive-aversive conditioning in controlled laboratory conditions (Whitney et al. 2009c), despite the fact that structural colours might corrupt colour identity due to changing appearance from different viewing angles (Whitney et al. 2016). ...
... For example, by using photography and a polarizing filter to remove gloss reflected from the surface of food there is a change in our perception of the colour of fruit (Landy 2007;Motoyoshi et al. 2007). The perceived colour of glossy surfaces is thus potentially a mixture of light changing in its wavelength composition after absorption by pigments, backscattering, and light unchanged in its wavelength composition after reflection from the surface (van der Kooi et al. 2017. ...
... As a result of the conical epidermis shape, the reflected light from the mesophyll may also scatter and diffuse light which can produce a velvet and matte texture of the petal (Kay et al. 1981;Kay 1988;Glover & Martin 1998). In contrast, flat surfaces produce a uniform and directional reflection of incident light, which may be perceived as gloss dependent of the viewing angle (Kay et al. 1981;Kay 1988;van der Kooi et al. 2014;van der Kooi et al. 2017). Gloss is largely independent of the wavelength, but strongly dependent on the angle of the incident light, and causes "whitish" reflections likely to be a dynamic component of flower petals when the flower visitor changes its position relative to the glossy surface (Hurlbert 2007;Land 1977;Skorpski & Chittka 2011). ...
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Colour signals of flowers facilitate detection, spontaneous preference, discrimination and flower constancy by important bee pollinators. At short distances bees orient to floral colour patterns to find a landing platform and collect nutrition, potentially improving the plants' reproductive success when multiple flowers are visited sequentially. In addition to pigments and backscattering structures within the petals' internal layers, the epidermal micro-structure of the petals' surface may also influence petal reflectance properties and thus influence overall colour patterns via optical effects. Gloss, i.e., shine caused by specular reflections of incident light from smooth surfaces, may for example alter the visual appearance of surfaces including flowers. We classify the epidermal surface properties of petals from 39 species of flowering plants from 19 families by means of a cell shape index, and measure the respective surface spectral reflectance from different angles. The spontaneous behavioural preferences of free flying bumblebees (Bombus terrestris) for surfaces with different micro-textures was then tested using specially prepared casts of selected flower petals. We specifically tested how the petal colour as function of the angle of incident light, surface structure and bee approach angle influences bumblebees' spontaneous choices for artificial flowers. We observe that bumblebees spontaneously prefer artificial flowers with conical-papillate micro-structures under both multidirectional illumination and under spotlight conditions if approaching against the direction of spotlight, suggesting conical cells help promote constant signals by removing gloss that may confound the integrity of colour signalling.
... However, reflectance amplitude depends both upon pigmentary coloration and on petal structure (van der and that structure characterizes some clades (e.g. Ranunculus, van der Kooi et al., 2017). Differences between clades might possibly be due to differences in petal structure. ...
Article
The high variability observed in floral traits has been interpreted as resulting from the adaptation of plants to pollinators, as the latter present innate preferences for specific floral traits and impose selection over them. However, some pollinators such as bees can learn to associate floral signals with rewards, thus increasing floral constancy on more rewarding flowers. The integration of all these rewards and cues is markedly important at community level, where co-flowering species compete for pollinators. In order to verify the honesty of the above-mentioned signals, we examined the association between floral visual signals (size, colour, symmetry and floral display) and rewards (pollen and nectar) for 98 species in a Mediterranean community. The associations between floral traits were analysed considering the phylogenetic relationship between the different species. Flower colour, size, pollen volume or amount of sucrose exhibited no phylogenetic signal, which suggests an adaptive evolution in response to different conditions in the pollinator community. Flower size was seen to constitute the most honest signal for pollinators, as this was significantly associated with quantities of pollen and nectar. In contrast, nectar concentration was observed to be positively associated with chromatic contrast. We detected no relationship between flower shape and rewards, on the one hand, nor between flower display and rewards, on the other. Our study unequivocally demonstrates the correlation between rewards and the visual signals perceived by bees, the most effective pollinators in the Mediterranean Basin. In the community studied, bees employed flower size at longer distances and chromatic contrast at shorter distances to predict rewards. The limited number of studies existing in this sense indicates that this kind of association appears to be community specific. A free Plain Language Summary can be found within the Supporting Information of this article.
... For instance, the glossy yellow petals of buttercups and lesser celandine have a very thin epidermis filled with yellow carotenoid pigments and innermost layers containing starch granules (Figure 3(b)). The thin epidermis acts as a film that reflects light, and the backscattering starch layer enhances brilliance, the two combined creating a gloss effect (Vignolini et al. 2012;van der Kooi et al. 2017). A similar phenomenon is observed in the California poppy (Eschscholzia californica Cham.) whose petals owe their bright orange colour to carotenoids and their silky aspect to the dense network of thin parallel ridges striating the epidermis (Wilts et al. 2018). ...
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Flowers are the flagship structure of angiosperms (flowering plants). This spectacular innovation has probably contributed in a significant way to the extraordinary success of angiosperms, which today make up 90% of land plant species. Flowering plants display a beautiful and spectacular diversity of floral forms that results largely from the diversification of reproductive strategies, including co-adaptation with pollinators. One of the most spectacular variations concerns flower colour, with an almost endless range of shades varying from pure white to near black. In many plants, floral colours contrast with the rest of the plant, and are generally produced by the presence of pigments other than chlorophyll, although in some cases colour is created by light-reflecting structures. The biosynthetic pathways of carotenoids, anthocyanins and betalains, the three main classes pigment, have been deciphered. In many species, flower colour plays a key role in pollination as a visual cue to attract biotic pollinators. Although petals are often the most colourful and showy part of the flower, there are many exceptions, including examples where bracts are showier than the flowers themselves. Colour is usually stable within a species, resulting from adaptive processes linked to plant-pollinator relationships. The evolutionary and genetic mechanisms involved in flower colour shifts have been described in several taxa, providing insights into some of the processes that have shaped the diversity of flowering plants.
... Furthermore, a previous study of buttercup (Ranunculus spp.) flowers [23] revealed that in addition to matte yellow flowers with little smoothness, buttercup also has yellow flowers with mirror-like reflectiveness. Using microscopic spectrophotometry and anatomical approaches, the researchers discovered the optical features of waxy flowers. ...
... There are three types of epidermal cell shapes in flowers distinguished by their shape. Flat cells are the least common type, but are characteristic of flowers in the buttercup genera Ranunculus and Ficaria (Ranunculaceae) contributing to their glossy appearance (Kay et al. 1981;Vignolini et al. 2012;van der Kooi et al. 2017). More common type of shapes are convex and cone-shaped ( Figure 1). ...
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The epidermal cells of flowers come in different shapes and have different functions, but how they evolved remains largely unknown. Floral micro‐texture can provide tactile cues to insects, and increases in surface roughness by means of conical (papillose) epidermal cells may facilitate flower handling by landing insect pollinators. Whether flower microstructure correlates with pollination mechanism remains unknown. Here, we investigate the floral epidermal microstructure in 29 (congeneric) species‐pairs with contrasting pollination mechanisms. We test whether flowers pollinated by bees or flies feature more structured, rougher surfaces than flowers pollinated by non‐landing moths or birds and flowers that self‐pollinate. In contrast with earlier studies, we find no correlation between epidermal microstructure and pollination mechanism. The shape, cell height and roughness of floral epidermal cells varies among species, but is not correlated with pollinators at large. Intriguingly however, we find that the upper (adaxial) flower surface that surrounds the reproductive organs and often constitutes the floral display is markedly more structured than the lower (abaxial) surface. We thus conclude that conical epidermal cells probably play another role in plant reproduction, such as increasing hydrophobicity or enhancing the visual signal.