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Floral colour

Goal: Floral colour evolution in angiosperms

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Jurene E Kemp
added 3 research items
Background and aims: As most plants rely on pollination for persistence in communities, pollination interactions should be important determinants of plant community assembly. Here, trait and phylogenetic null modelling approaches were combined with pollinator interaction networks to elucidate the processes structuring flower colour assembly patterns in Asteraceae communities in Namaqualand, South Africa. Methods: Plant species were assigned to flower colour pattern categories (CPCs) that incorporate the complexity of the bulls-eye colour pattern, using pollinator vision models. Null models were used to assess whether daisy communities exhibit clustering (driven by filtering, facilitation or convergence) or overdispersion (driven by competitive exclusion or character displacement) of CPCs. Next, flower visitor networks were constructed for communities with non-random CPC assembly to confirm the functional role of pollinators in determining floral trait assembly. Key results: Plant species are unevenly distributed across CPCs, the majority of which are not phylogenetically conserved, suggesting that certain CPCs have a selective advantage. Clustering of CPCs in communities is more frequent than overdispersion, and this does not reflect non-random phylogenetic assembly. In most communities at least one CPC is overrepresented relative to null assemblages. Interaction networks show that each community has a single dominant pollinator that strongly interacts with the overrepresented CPC, suggesting a role for pollinator preferences in driving clustered assembly of CPCs within daisy communities. Conclusion: This novel approach, which demonstrates non-random assembly of complex flower colour patterns and corroborates their functional association with particular pollinators, provides strong evidence that pollinators influence plant community assembly. Results suggest that in some community contexts the benefits of pollinator sharing outweigh the costs of heterospecific pollen transfer, generating clustered assembly. They also challenge the perception of generalized pollination in daisies, suggesting instead that complex daisy colour patterns represent a pollination syndrome trait linked to specific fly pollinators.
Floral apparency is shaped by both mutualistic and antagonistic interactions that can act in opposing ways. Pollinators are expected to select for more visually apparent flowers, but this likely trades off against the potentially severe fitness costs of damage to apparent flowers by floral herbivores. One way in which flowers that close during parts of the day might circumvent this trade‐off is by evolving less visible lower petal surfaces that are inconspicuous to herbivores when flowers are closed. Here, we used visual system modelling and herbivory experiments to test whether petal surfaces that are exposed when flowers are closed are cryptically coloured. We collected lower and upper petal surface spectra for 77 Asteraceae species from Namaqualand, South Africa. This included closing species that expose their lower petal surfaces for 5–6 daylight hours and non‐closing species that do not expose their lower surfaces. We used these contrasting groups to test the expectation of reduced conspicuousness of lower petal surfaces in closing, but not non‐closing species. By modelling reflectance spectra of petal surfaces against a green leaf background in various visual systems, we showed (a) that conspicuousness of upper petal surfaces to pollinators and various herbivores was strongly correlated, suggesting the potential for fitness trade‐offs between attracting mutualists and antagonists to open flowers, (b) that closing species' lower petal surfaces were less visible to herbivores against a leaf background than those of non‐closing species and (c) that closing species had larger differences between upper and lower petal surface coloration than non‐closing species. Behavioural experiments with tortoise herbivores demonstrated that flowers are easily detected when upper surfaces are exposed, but that tortoises were unable to distinguish lower petal surfaces against a leaf background, resulting in reduced flower herbivory. These results are consistent with selection by herbivores for cryptic coloration of lower petal surfaces, and divergence of coloration between lower and upper petal surfaces in species with closing flowers. Visual crypsis of flowers may be an effective anti‐herbivory strategy during times when pollinators are inactive, and provides an alternative to chemical defence, which often involves costs to pollination. A free Plain Language Summary can be found within the Supporting Information of this article. A free Plain Language Summary can be found within the Supporting Information of this article.
The striking variation in flower color across and within Angiosperm species is often attributed to divergent selection resulting from geographic mosaics of pollinators with different color preferences. Despite the importance of pollinator mosaics in driving floral divergence, the distributions of pollinators and their color preferences are seldom quantified. The extensive mass-flowering displays of annual daisy species in Namaqualand, South Africa, are characterized by striking color convergence within communities, but also color turnover within species and genera across large geographic scales. We aimed to determine whether shifts between orange and white-flowered daisy communities are driven by the innate color preferences of different pollinators or by soil color, which can potentially affect the detectability of different colored flowers. Different bee-fly pollinators dominated in both community types so that largely non-overlapping pollinator distributions were strongly associated with different flower colors. Visual modeling demonstrated that orange and white-flowered species are distinguishable in fly vision, and choice experiments demonstrated strongly divergent color preferences. We found that the dominant pollinator in orange communities has a strong spontaneous preference for orange flowers, which was not altered by conditioning. Similarly, the dominant pollinator in white communities exhibited an innate preference for white flowers. Although detectability of white flowers varied across soil types, background contrast did not alter color preferences. These findings demonstrate that landscape-level flower color turnover across Namaqua daisy communities is likely shaped by a strong qualitative geographic mosaic of bee-fly pollinators with divergent color preferences. This is an unexpected result given the classically generalist pollination phenotype of daisies. However, because of the dominance of single fly pollinator species within communities, and the virtual absence of bees as pollinators, we suggest that Namaqua daisies function as pollination specialists despite their generalist phenotypes, thus facilitating differentiation of flower color by pollinator shifts across the fly pollinator mosaic.
Casper J Van der Kooi
added 7 research items
Flavonoid pigments are key determinants of flower colors. As absorption spectra of flavonoids are known to be severely pH-dependent, cellular pH will play a crucial role in flower coloration. The flavonoids are concentrated in the vacuoles of the flowers’ epidermal cells, and thus the pigments’ absorption spectra are modulated by the vacuolar pH. Here we study the pH dependence of flavonoid absorption spectra in extracts from flowers of two poppy species Papaver dubium (red) and Meconopsis cambrica (orange), and a white and red Mandevilla sanderi variety. In the red poppy and Mandevilla flowers, absorption spectra of the cyanidin- and pelargonidin-based anthocyanins peak in the blue-green-wavelength range at low pH, but exhibit a distinct bathochromic shift at higher pH. This shift to longer wavelengths is not found for the blue-absorbing nudicaulin derivatives of M. cambrica , which have a similar absorption spectrum at low and high pH. The pH-dependent absorption changes of the white M. sanderi ’s flavonoid remained restricted to the UV. An analysis of the spectra with logistic functions suggests that the pH-dependent characteristics of the basic states of flavonols and anthocyanins are related. The implications of tuning of pH and pigment absorption spectra for studies on flower color evolution are discussed.
Nutrient deficiency is known to constrain plant growth in numerous ways, but how it impacts floral displays and pollination success remains unclear. Here we investigate how insufficient availability of sulphur-a vital plant nutrient that is a limiting factor in natural and agricultural regions throughout the world-influences the production of floral displays in Brassica rapa, Physalis philadelphica and three Petunia species with differently coloured flowers. Sulphur deficiency led to a drastic reduction in the number of open flowers, an aberrant flower morphology and smaller pollen with an altered mineral nutrient content. Intriguingly, sulphur deprivation also led to a clear reduction in pigmentation of yellow flowers, but not in flowers with white, purple and red colours. The pale yellow flower colour was due to decreased amounts of violaxanthin, lutein and other carotenoids, suggesting that the carotenoid synthesis pathway is particularly susceptible to sulphur deficiency. Additional experiments with nitrogen and phosphorus depletion confirmed that observed colour and morphological changes were not a general nutrient limitation response, but could be ascribed to sulphur depletion specifically. Taken together, our results showed that (mild) sulphur deficiency deteriorates a suite of floral traits, and that the effects may cascade to pollinators and so have the potential to undermine (agro-)ecosystem functioning.
The flowers of poppies (Papaveraceae) exhibit bright colours, despite their thin and floppy petals. We investigated the optical properties of flowers of Papaver rhoeas, P. dubium, Meconopsis cambrica and Argemone polyanthemos using a combined approach of anatomy, spectrophotometry and optical modelling. The petals of Papaver flowers are composed of only three cell layers, an upper and lower epidermal layer, which are densely filled with pigment, and an unpigmented mesophyll layer. Dense pigmentation together with strong scattering structures, composed of serpentine cell walls and air cavities, cause the striking poppy colours. We discuss how various aspects of the optical signal contribute to the flower’s visibility to pollinators.
Klaus Lunau
added a research item
Blumen sind Kommunikationsstrukturen zwischen Blütenpflanzen und ihren Bestäubern. Dabei spielen visuelle Farbsignale eine herausragende Rolle. Da kein Bestäuber über ein dem Menschen ähnliches Farbsehsystem verfügt, beruht das Verstehen von Blumenfarben auf einer Analyse mit den Augen des betrachtenden Blütenbesuchers. Ultraviolettes Licht hat dabei eine Sonderstellung, da es für Menschen unsichtbar, für die meisten Blütenbesucher aber wahrnehmbar und eine von vielen Blüten ausgebildete Farbkomponente bildet. UV kann zu Kommunikation zwischen Blüte und Bestäuber entscheidend beitragen. UV- Muster auf Blüten schützen Pollen vor UV-Strahlung und sind gleichzeitig wegweisende Strukturen, mit deren Hilfe Blütenbesucher einen Landeplatz und eine Belohnung finden und gleichzeitig so manipuliert werden, dass die Übertragung von Pollen auf den Bestäuber oder von diesem auf die Narbe anderer Blüten wahrscheinlicher wird. Blütenfarbmuster, die durch Glanz erzeugt werden, können auf sichtbar glänzenden Nektar hinweisen oder diesen vortäuschen. Mit UV-Aufnahmen und Falschfarbenfotos in Bienensicht wird die Bedeutung ultravioletter Farbkomponenten auf Blüten deutlich gemacht.
Mani Shrestha
added 2 research items
Although angiosperms exhibit a wide range of variability in floral traits such as shape and size, flower color is a hallmark of angiosperm diversity. Since before Darwin's time, flower color has long been appreciated for its role in pollinator attraction (Sprengel, 1793; Mendel, 1866; Darwin, 1895; Faegri and van der Pijl, 1966; Proctor and Yeo, 1973). However, over the past few decades, a growing body of evidence suggests that flower color can be molded by a diversity of selective pressures. The rapid accumulation of flower color studies has spurred several thorough reviews (Winkel-Shirley, 2001; Koes et al., 2005; Rausher, 2008; Sobel and Streisfeld, 2013; Narbona et al., 2018; Sapir et al., 2021), but here we present the largest collection of investigations specifically focused on the role of flower color in angiosperm evolution. This Research Topic is composed of 28 studies on the role of flower color in angiosperm evolution. These contributions include species living on nearly all continents plucked from most major branches of the angiosperm tree of life (Figure 1). Investigations span traditional scales in biology, from gene expression and biochemical profiles to pollinator perception and community assembly. Evolutionarily, studies range from within species flower color polymorphisms to macroevolutionary patterns of flower color evolution within and among genera. Ecologically, investigations span a diversity of plant communities including neotropical savannas, temperate serpentine seeps, subtropical mountains, and tropical dry forests.
• Bees are major pollinators of angiosperms and have phylogenetically conserved colour vision but differ in how various key species use achromatic information that is vital for both flower detection and size processing. • We modelled green contrast and colour contrast signals from flowers of different countries where there are well established differences in availability of model bee species along altitudinal gradients. We tested for consistency in visual signals as expected from generalization in pollination principles using phylogenetically informed linear models. • Patterns of chromatic contrast, achromatic green contrast and flower size differed among the three floras we examined. In Nepal there is a significant positive correlation between flower size and colour contrast in the subalpine region, but a negative correlation at the lower altitudes. At high elevations in Norway, where pollinators other than bees are common, flower size was positively correlated with colour contrast. At low and medium altitudes in Norway and in Australia, we did not observe a significant relationship between size and colour contrast. • We thus find that the relationship between size, green and colour contrast cannot be generalized across communities, thus suggesting that flower visual signal adaptations to local pollinators are not limited to chromatic contrast.
Mani Shrestha
added a research item
Plant‐pollinator interactions provide a natural experiment in signal evolution. Flowers are known to have evolved colour signals that maximise their ease of detection by the visual systems of important pollinators like bees. Whilst most angiosperms are bee pollinated, our understanding on how the second largest group of pollinating insects, flies, may influence flower colour evolution is limited to the use of categorical models of colour discrimination that do not reflect the small colour differences commonly observed between and within flower species. Here we show by comparing flower signals that occur in different environments including total absence of bees, a mixture of bee and fly pollination within one plant family (Orchidaceae) from a single community, and typical flowers from a broad taxonomic sampling of the same geographic region, that perceptually different colours do evolve in response to different types of insect pollinator. We show evidence of both convergence among fly‐pollinated floral colours but also of divergence and displacement of colour signals in the absence of bee pollinators. Our findings give an insight into how both ecological and agricultural systems may be affected by changes in pollinator distributions around the world.
Zong-Xin Ren
added a research item
The evolution of floral traits in animal-pollinated plants involves the interaction between flowers as signal senders and pollinators as signal receivers. Flower colors are very diverse, effect pollinator attraction and flower foraging behavior, and are hypothesized to be shaped through pollinator-mediated selection. However, most of our current understanding of flower color evolution arises from variation between discrete color morphs and completed color shifts accompanying pollinator shifts, while pollinator-mediated selection on continuous variation in flower colors within populations is still scarce. In this review, we summarize experiments quantifying selection on continuous flower color variation in natural plant populations in the context of pollinator interactions. We found that evidence for significant pollinator-mediated selection is surprisingly limited among existing studies. We propose several possible explanations related to the complexity in the interaction between the colors of flowers and the sensory and cognitive abilities of pollinators as well as pollinator behavioral responses, on the one hand, and the distribution of variation in color phenotypes and fitness, on the other hand. We emphasize currently persisting weaknesses in experimental procedures, and provide some suggestions for how to improve methodology. In conclusion, we encourage future research to bring together plant and animal scientists to jointly forward our understanding of the mechanisms and circumstances pollinator-mediated selection on flower color.
Mani Shrestha
added a research item
The majority of angiosperms require animal pollination for reproduction and insects are the dominant group of animal pollinators. Bees are considered one of the most important and abundant insect pollinators. Research into bee behaviour and foraging decisions has typically centred on managed eusocial bee species, Apis mellifera and Bombus terrestris. Non-eusocial bees are understudied with respect to foraging strategies and decision-making, such as flower preferences. Understanding whether there are fundamental foraging strategies and preferences which are features of insect groups can provide key insights into the evolution of flower-pollinator co-evolution. In the current study, Lasioglossum (Chilalictus) lanarium and L. (Parasphecodes) sp., two native Australian generalist halictid bees, were tested for flower shape preferences between native insect-pollinated and bird-pollinated flowers. Each bee was presented with achromatic images of either insect-pollinated or bird-pollinated flowers in a circular arena. Both native bee species demonstrated a significant preference for images of insect-pollinated flowers. These preferences are similar to those found in A. mellifera, suggesting that flower shape preference may be a deep-rooted evolutionary occurrence within bees. With growing interest in the sensory capabilities of non-eusocial bees as alternative pollinators, the current study also provides a valuable framework for further behavioural testing of such species.
Klaus Lunau
added a research item
A c c e p t e d M a n u s c r i p t 2  Background and Aims Colour pattern is a key cue of bee attraction selectively driving the appeal of pollinators. It comprises the main colour of the flower with extra fine patterns indicating a reward focal point such as nectar, nectaries, pollen, stamens, and floral guides. Such definition of floral traits' advertisement guides visitation by the insects, assuring precision in pollen gathering and deposition. The study, focused in Southwest Australian Floristic Region (SWAFR), aimed to spot bee colour patterns that are usual and unusual, missing, accomplished by mimicry of pollen and anthers; and overlapped between mimic-model species in floral mimicry cases.  Methods Floral colour patterns were examined by false colour photography in 55 flower species of multiple highly diverse natural plant communities in southwest Australia. False colour photography is a method to transform a UV-photo and a colour photo into a false colour photo based on trichromatic vision of bees. This method results particularly effective for rapid screening of large numbers of flowers for the presence of fine-scale bee-sensitive structures and surface roughage that are not detectable using standard spectrophotometry.  Key Results Bee-, and bird-pollinated flowers showed expected but also some remarkable and unusual previously undetected floral colour pattern syndromes. Typical colour patterns include cases of pollen and flower mimicry and ultraviolet-absorbing targets. Among the atypical floral colour patterns are unusual white and UV-reflecting flowers of bee-pollinated plants, bicoloured floral guides, consistently occurring in Fabaceae spp., and flowers displaying a selective attractiveness to birds only. In orchids' genera (Diuris and Thelymitra) that employ floral mimicry of model species we revealed a surprising mimicry phenomenon of anthers mimicked in turn by models species. Conclusion The study demonstrates the applicability of 'bee view' colour imaging for deciphering pollinator cues in a biodiverse flora with potential to be applied to other eco regions. The technique provides an exciting opportunity for indexing floral traits on a biome-scale to establish pollination drivers of ecological and evolutionary relevance.
Klaus Lunau
added a research item
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.
Kazuharu Ohashi
added a research item
Explanations of floral adaptation to diverse pollinator faunas have often invoked visitor-mediated trade-offs in which no intermediate, generalized floral phenotype is optimal for pollination success, i.e. fitness valleys are created. In such cases, plant species are expected to specialize on particular groups of flower visitors. Contrary to this expectation, it is commonly observed that flowers interact with various groups of visitors, while at the same time maintaining distinct phenotypes among ecotypes, subspecies, or congeners. This apparent paradox may be due to a gap in our understanding of how visitor-mediated trade-offs could affect floral adaptation. Here we provide a conceptual framework for analysing visitor-mediated trade-offs with the hope of stimulating empirical and theoretical studies to fill this gap. We propose two types of visitor-mediated trade-offs to address negative correlations among fitness contributions of different visitors: visitor-mediated phenotypic trade-offs (phenotypic trade-offs) and visitor-mediated opportunity trade-offs (opportunity trade-offs). Phenotypic trade-offs occur when different groups of visitors impose conflicting selection pressures on a floral trait. By contrast, opportunity trade-offs emerge only when some visitors’ actions (e.g. pollen collection) remove opportunities for fitness contribution by more beneficial visitors. Previous studies have observed disruptive selection due to phenotypic trade-offs less often than expected. In addition to existing explanations, we propose that some flowers have achieved ‘adaptive generalization’ by evolving features to avoid or eliminate the fitness valleys that phenotypic trade-offs tend to produce. The literature suggests a variety of pathways to such ‘trade-off mitigation’. Trade-off mitigation may also evolve as an adaptation to opportunity trade-offs. We argue that active exclusion, or floral specialization, can be viewed as a trade-off mitigation, occurring only when flowers cannot otherwise avoid strong opportunity trade-offs. These considerations suggest that an evolutionary strategy for trade-off mitigation is achieved often by acquiring novel combinations of traits. Thus, phenotypic diversification of flowers through convergent evolution of certain trait combinations may have been enhanced not only through adaptive specialization for particular visitors, but also through adaptive generalization for particular visitor communities. Explorations of how visitor-mediated trade-offs explain the recurrent patterns of floral phenotypes may help reconcile the long-lasting controversy on the validity of pollination syndromes.
Mani Shrestha
added a research item
Pollinators with different vision are a key driver of flower coloration. Islands provide important insights into evolutionary processes, and previous work suggests islands may have restricted flower colors. Due to both species richness with high endemism in tropical-subtropical environments, and potentially changing pollinator distributions with altitude, we evaluated flower color diversity across the mountainous island of Taiwan in a comparative framework to understand the cause of color diversity. We sampled flower color signaling on the tropical-subtropical island of Taiwan considering altitudes from sea level to 3300 m to inform how over-dispersion, random processes or clustering may influence flower signaling. We employed a model of bee color space to plot loci from 727 species to enable direct comparisons to data sets from continental studies representing Northern and Southern Hemispheres, and also a continental mountain region. We observed that flower color diversity was similar to flowers that exist in mainland continental studies, and also showed evidence that flowers predominantly had evolved color signals that closely matched bee color preferences. At high altitudes floras tend to be phylogenetically clustered rather than over-dispersed, and their floral colors exhibited weak phylogenetic signal which is consistent with character displacement that facilitated the coexistence of related species. Overall flower color signaling on a tropical-subtropical island is mainly influenced by color preferences of key bee pollinators, a pattern consistent with continental studies.
Klaus Lunau
added a research item
Signals from flowers attract pollinators, usually with a mutualistic relationship giving reciprocal benefits. However, this relationship carries with it many pitfalls, including various kinds of deception in flowers and illegitimate visits of flower visitors or flower antagonists (van der Kooi et al., 2019). Flowers do not benefit from attracting as many flower visitors as possible, but select among potential flower visitors, since visual, tactile and olfactory floral cues can selectively allure pollinators and distract floral antagonists including pollen thieves, nectar robbers and florivores. That the exclusion of antagonistic flower visitors is not a local phenomenon of a few species is shown by Chen et al. (2020), who provide evidence that the exclusion of bees from bird-pollinated flowers via a private colour channel is a global phenomenon.
Klaus Lunau
added a research item
Das Farbensehen des Menschen ist nicht mit dem Farbensehen von blütenbesuchenden Bienen zu vergleichen, denn Bienen können ultraviolettes Licht sehen, sind aber unempfindlich für rotes Licht. UV-Photos lassen spezielle, nur im UV sichtbare Muster auf Blüten erkennen. Durch den Vergleich mit Farbphotos gewinnt man eine Vorstellung, wie Bienen die Blüte wahrnehmen. Als Alternative hierfür wird die Falschfarbenphotographie in Bienensicht vorgestellt. Bei dieser wird nicht nur der ultraviolette Wellenlängenbereich erfasst, sondern auch der Rotanteil bleibt unberücksichtigt. Um dem Betrachter einen Farbeindruck zu vermitteln, wird als Codierung eine Darstellung von UV als Blau, von Blau als Grün und von Grün als Rot vorgeschlagen. Die so visualisierten Blumenfarbmuster sind eingängig und erleichtern die Interpretation, zumal selbst kleinste Details wie Staubgefäße und Pollenkörner klar hervortreten. Die Falschfarbenphotographie erfordert eine modifizierte Digitalkamera, ein UV-durchlässiges Objektiv, Filter für einzelne Wellenlängenbereiche und ein Stativ.
Mani Shrestha
added a research item
Innate colour preferences promote the capacity of pollinators to find flowers, although currently there is a paucity of data on how preferences apply to real flowers. The Australian sugarbag bee (Tetragonula carbonaria Sm.) has innate preferences for colours, including UV-absorbing white. Sugarbag bees are pollinators of the terrestrial orchid Caladenia carnea R.Br., which has both white and pink morphs. In laboratory conditions, we tested flower-naïve bees with the white and pink flower morphs revealing a significant preference for the white morph, consistent with experiments using artificial stimuli. In experiments to understand how bees may select food-deceptive orchids following habituation to a particular colour morph, we observed a significant increase in choices towards novel white flowers. We also observed that the presence of a UV-reflecting dorsal sepal signal significantly increased bee choices compared to flowers that had the UV signal blocked. Our findings demonstrate that innate preference testing of insect pollinators with artificial stimuli is replicated in a biologically significant scenario with flowers. The findings also underscore how food-deceptive orchids can receive sufficient pollinator visits to ensure pollination by having different morphs that draw on the innate preferences of bees and their ability to make decisions in a complex ecological setting.
Mani Shrestha
added a research item
Abstract Background and Aims Pollinator-mediated interactions between plant species may affect the composition of angiosperm communities. Floral colour signals should play a role in these interactions, but the role will arise from the visual perceptions and behavioural responses of multiple pollinators. Recent advances in the visual sciences can be used to inform our understanding of these perceptions and responses. We outline the application of appropriate visual principles to the analysis of the annual cycle of floral colour structure in two Australian herbaceous communities. Methods We used spectrographic measurements of petal reflectance to determine the location of flowers in a model of hymenopteran colour vision. These representations of colour perception were then translated to a behaviourally relevant metric of colour differences using empirically calibrated colour discrimination functions for four hymenopteran species. We then analysed the pattern of colour similarity in terms of this metric in samples of co-flowering plants over the course of a year. We used the same method to analyse the annual pattern of phylogenetic relatedness of co-flowering plants in order to compare colour structure and phylogenetic structure. Key Results Co-flowering communities at any given date seldom had colour assemblages significantly different from random. Non-random structure, both dispersion and clustering, occurred occasionally, but depended on which bee observer is considered. The degree of colour similarity was unrelated to phylogenetic similarity within a co-flowering community. Conclusions Perceived floral colour structure varied with the sensory capabilities of the observer. The lack of colour structure at most sample dates, particularly the rarity of strong dispersion, suggests that plants do not use chromatic signals primarily to enable bees to discriminate between co-flowering species. It is more likely that colours make plants detectable in a complex landscape.
Mani Shrestha
added a research item
Klaus Lunau
added a research item
The colour vision system of bees and humans differs mainly in that, contrary to humans, bees are sensitive to ultraviolet light and insensitive to red light. The synopsis of a colour picture and a UV picture is inappropriate to illustrate the bee view of flowers, since the colour picture does not exclude red light. In this study false-colour pictures in bee view are assembled from digital photos taken through a UV, a blue, and a green filter matching the spectral sensitivity of the bees' photoreceptors. False-colour pictures demonstrate small-sized colour patterns in flowers, e.g. based on pollen grains, anthers, filamental hairs, and other tiny structures that are inaccessible to spectrophotometry. Moreover, false-colour pictures are suited to demonstrate flowers and floral parts that are conspicuous or inconspicuous to bees. False-colour pictures also direct the attention to other ranges of wavelength besides ultraviolet demonstrating for example blue and yellow bulls' eyes in addition to UV bulls' eyes which previously have been overlooked. False-colour photography is a robust method that can be used under field conditions, with various equipment and with simple colour editing.
Mani Shrestha
added a project goal
Floral colour evolution in angiosperms
 
Mani Shrestha
added 2 research items
Angle dependent colours, such as iridescence, are produced by structures present on flower petals changing their visual appearance. These colours have been proposed to act as signals for plant-insect communication. However, there is a paucity of behavioural data to allow for interpretations of how to classify these colours either as a signal or a cue when considering the natural conditions under which pollination occurs. We sampled flowers from six plant species across various viewpoints looking for changes in the visual appearance of the petals. Spectral characteristics were measured with different instruments to simulate both the spectral and spatial characteristics of honeybee’s vision. We show the presence of colour patches produced by angle dependent effects on the petals and the calyx of various species; however, the appearance of the angle dependent colour patches significantly varies with viewpoint and would only be resolved by the insect eye at close distances. Behaviour experiments with honeybees revealed that pollinators did not use angle dependent colours to drive behaviour when presented with novel flower presentations. Results show that angle dependent colours do not comply with the requirements of a signal for plant-pollinator communication since the information transmitted by these colours would be unreliable for potential, free-flying pollination vectors. We thus classify angle dependent colours produced by micro- and ultra-structures as being a cue (a feature which has not evolved for communication), and observe no evidence supporting claims of these angle dependent colours having evolved as visual signal.
Plant-pollinator interactions have a fundamental influence on flower evolution. Flower colour signals are frequently tuned to the visual capabilities of important pollinators such as either bees or birds, but far less is known about whether flower shape influences the choices of pollinators. We tested European honeybee (Apis mellifera) preferences using novel achromatic (grey-scale) images of 12 insect-pollinated and 12 bird-pollinated native Australian flowers in Germany; thus avoiding influences of colour, odour or prior experience. Independent bees were tested with a number of parameterised images specifically designed to assess preferences for size, shape, brightness, or the number of flower-like shapes present in an image. We show that honeybees have a preference for visiting images of insect-pollinated flowers and such a preference is most-likely mediated by holistic information rather than by individual image parameters. Our results indicate angiosperms have evolved flower shapes which influence the choice behaviour of important pollinators, and thus suggest spatial achromatic flower properties are an important part of visual signalling for plant-pollinator interactions.
Mani Shrestha
added 9 research items
One hundred years ago it was often assumed that the capacity to perceive colour required a human brain. Then in 1914 a young Austrian researcher working at Munich University in Germany published evidence that honeybees could be trained to collect sugar water from a 'blue' coloured card, and find the colour among a number of different shades of achromatic grey. Von Frisch thus established honeybees as an important model of sensory processing in animals, and for work including his demonstration that bees used a symbolic dance language, won a Nobel Prize in 1973. This work led to the establishment of several research groups in Germany that developed a rich understanding of how bee vision has shaped flower colour evolution in the Northern Hemisphere. Applying these insights to Australian native bees offers great insights due to the long-term geological isolation of the continent. Australian bees have a phylogenetically ancient colour visual system and similar colour perception to honeybees. In Australia similar patterns of flower colour evolution have resulted and provide important evidence of parallel evolution, thanks to the pioneering work of Karl von Frisch 100 years ago.
Colour signals are a major cue in putative pollination syndromes. There is evidence that the reflectance spectra of many flowers target the distinctive visual discrimination abilities of hymenopteran insects, but far less is known about bird-pollinated flowers. Birds are hypothesized to exert different selective pressures on floral colour compared with hymenopterans because of differences in their visual systems. We measured the floral reflectance spectra of 206 Australian angiosperm species whose floral visitors are known from direct observation rather than inferred from floral characteristics. We quantified the match between these spectra and the hue discrimination abilities of hymenopteran and avian vision, and analysed these metrics in a phylogenetically informed comparison of flowers in different pollination groups. We show that bird-visited flowers and insect-visited flowers differ significantly from each other in the chromatic cues they provide, and that the differences are concentrated near wavelengths of optimal colour discrimination by whichever class of pollinator visits the flowers. Our results indicate that angiosperms have evolved the spectral signals most likely to reinforce their pollinators' floral constancy (the tendency of individual pollinators to visit flowers of the same species) in communities of similarly coloured floral competitors.
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. Differences in colour diversity between zones may reflect differences in the ecologically available morphospace based on pollinator species richness and the constancy of their foraging behaviour. The chromatic signals present in Nepali species are similar to the signals found in insect-pollinated floras of other regions of the world.
Mani Shrestha
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Orchids are a classic angiosperm model for understanding biotic pollination. We studied orchid species within two species‐rich herbaceous communities that are known to have either hymenopteran or dipteran insects as the dominant pollinators, in order to understand how flower colour relates to pollinator visual systems. We analysed features of the floral reflectance spectra that are significant to pollinator visual systems and used models of dipteran and hymenopteran colour vision to characterize the chromatic signals used by fly‐pollinated and bee‐pollinated orchid species. In contrast to bee‐pollinated flowers, fly‐pollinated flowers had distinctive points of rapid reflectance change at long wavelengths and a complete absence of such spectral features at short wavelengths. Fly‐pollinated flowers also had significantly more restricted loci than bee‐pollinated flowers in colour space models of fly and bee vision alike. Globally, bee pollinated flowers are known to have distinctive, consistent colour signals. Our findings of different signals for fly pollination is consistent with pollinator‐mediated selection on orchid species that results from the distinctive features of fly visual systems. This article is protected by copyright. All rights reserved.
Mani Shrestha
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Color discrimination thresholds proposed by receptor-noise type models are frequently used in animal vision studies to predict a precise limit on the capacity of an animal to discriminate between stimuli. Honeybees and bumblebees are 2 closely related hymenopteran species for which precise data on photoreceptor sensitivities and receptor noise exist, enabling accurate testing on how their vision conforms to model predictions. Color vision has been proved in these species, and they are known to predominantly visit flowers using visual signals to collect nutrition. Surprisingly, however, the natural variability of flower signals has been rarely considered, and recent work also suggests bees may tune color vision through experience. We initially measured the spectral variability of flowers from 2 species: Goodenia ovata and Rosemarinus officinalis where free-flying honeybees were observed constantly foraging from conspecific flowers. We empirically determined honeybee color discrimination thresholds for color stimuli considering either absolute- or differential-conditioning discrimination functions. Secondly, we analyzed greenhouse grown wild-type Antirrhinum majus flower petal spectra as well as spectra from mixta and nivea strains of this species, and empirically determined bumblebee color discrimination considering conditioning experience. In all measured cases, within-flower type spectral variability exceeded a 1.0 Receptor Noise threshold, often by several units. Observed behavioral color discrimination functions considering the respective conditioning procedures closely matched the range of signal variability for both honeybees and bumblebees, showing that color vision in bees cannot be described by a single fixed value, and plasticity is a key component of bee foraging behavior in natural environments.