Ancient insect vision tuned for flight among rocks and plants underpins natural flower colour diversity.

Understanding the origins of flower colour signalling to pollinators is fundamental to evolutionary biology and ecology. Flower colour evolves under pressure from visual systems of pollinators, like birds and insects, to establish global signatures among flowers with similar pollinators. However, an understanding of the ancient origins of this relationship remains elusive. Here, we employ computer simulations to generate artificial flower backgrounds assembled from real material sample spectra of rocks, leaves and dead plant materials, against which to test flowers' visibility to birds and bees. Our results indicate how flower colours differ from their backgrounds in strength, and the distributions of salient reflectance features when perceived by these key pollinators, to reveal the possible origins of their colours. Since Hymenopteran visual perception evolved before flowers, the terrestrial chromatic context for its evolution to facilitate flight and orientation consisted of rocks, leaves, sticks and bark. Flowers exploited these pre-evolved visual capacities of their visitors, in response evolving chromatic features to signal to bees, and differently to birds, against a backdrop of other natural materials. Consequently, it appears that today's flower colours may be an evolutionary response to the vision of diurnal pollinators navigating their world millennia prior to the first flowers.

Ant nests increase litter decomposition to mitigate the negative effect of warming in an alpine grassland ecosystem.

Warming can decrease feeding activity of soil organisms and affect biogeochemical cycles. The ant Formica manchu is active on the nest surface and prefers a hot, dry environment; therefore, warming may provide a favourable environment for its activities. We hypothesized that F. manchu benefit from warming and mitigate the negative effects of warming on litter decomposition. We examined the effects of ant nests (nest absence versus nest presence) and warming (+1.3 and +2.3°C) on litter decomposition, soil properties and the plant community in alpine grassland. Decomposition stations with two mesh sizes were used to differentiate effects of microorganisms (0.05 mm) and macroinvertebrates (1 cm) on decomposition. Ant nests increased litter decomposition with and without macroinvertebrates accessing the decomposition station when compared to plots without ant nests. Only litter decomposition in ant nests with macroinvertebrates having access to the decomposition station was not affected negatively by warming. Plots with ant nests had greater soil carbon, nutrient contents and plant growth than plots without ant nests, regardless of warming. Our results suggest that ant nests maintain ecosystem processes and functions under warming. Consequently, a management strategy in alpine grasslands should include the protection of these ants and ant nests.

Fly pollination drives convergence of flower coloration.

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 such as 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, empirically measured, do evolve in response to different types of insect pollinators. 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.

Spontaneous choices for insect-pollinated flower shapes by wild non-eusocial halictid bees.

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, including 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 that 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 Lasioglossum (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.

Colour preferences of Tetragonula carbonaria Sm. stingless bees for colour morphs of the Australian native orchid Caladenia carnea.

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.

Floral colour structure in two Australian herbaceous communities: it depends on who is looking.

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.

Why background colour matters to bees and flowers.

Flowers are often viewed by bee pollinators against a variety of different backgrounds. On the Australian continent, backgrounds are very diverse and include surface examples of all major geological stages of the Earth's history, which have been present during the entire evolutionary period of Angiosperms. Flower signals in Australia are also representative of typical worldwide evolutionary spectral adaptations that enable successful pollination. We measured the spectral properties of 581 natural surfaces, including rocks, sand, green leaves, and dry plant materials, sampled from tropical Cairns through to the southern tip of mainland Australia. We modelled in a hexagon colour space, how interactions between background spectra and flower-like colour stimuli affect reliable discrimination and detection in bee pollinators. We calculated the extent to which a given locus would be conflated with the loci of a different flower-colour stimulus using empirically determined colour discrimination regions for bee vision. Our results reveal that whilst colour signals are robust in homogeneous background viewing conditions, there could be significant pressure on plant flowers to evolve saliently-different colours to overcome background spectral noise. We thus show that perceptual noise has a large influence on how colour information can be used in natural conditions.

Coevolutionary elaboration of pollination-related traits in an alpine ginger (Roscoea purpurea) and a tabanid fly in the Nepalese Himalayas.

Geographical variation in the interacting traits of plant-pollinator mutualism can lead to local adaptive differentiation. We tested Darwin's hypothesis of reciprocal selection as a key driving force for the evolution of floral traits of an alpine ginger (Roscoea purpurea) and proboscis length of a tabanid fly (Philoliche longirostris). We documented the pattern of trait variation in R. purpurea and P. longirostris across five populations. At each site, we quantified pollinator-mediated selection on floral display area, inflorescence height and corolla length of R. purpurea by comparing selection gradients for flowers exposed to natural pollination and to supplemental hand pollination. Reciprocal selection between plant and fly was examined at two sites via the relationship between proboscis length and nectar consumption (fly benefit) and corolla length and pollen deposition (plant benefit). Local corolla tube length was correlated with local fly proboscis length among the five sites. We found strong linear selection imposed by pollinators on corolla tube length at all sites, but there was no consistent relationship of fitness to inflorescence height or floral display area. Selection between corolla length and proboscis length was reciprocal at the two experimental sites examined. The geographical pattern of trait variation and the evidence of selection is consistent with a mosaic of local, species-specific reciprocal selection acting as the major driving force for the evolution of corolla length of R. purpurea and proboscis length of P. longirostris.

Innate colour preferences of the Australian native stingless bee Tetragonula carbonaria Sm.

Innate preferences promote the capacity of pollinators to find flowers. Honeybees and bumblebees have strong preferences for 'blue' stimuli, and flowers of this colour typically present higher nectar rewards. Interestingly, flowers from multiple different locations around the world independently have the same distribution in bee colour space. Currently, however, there is a paucity of data on the innate colour preferences of stingless bees that are often implicated as being key pollinators in many parts of the world. In Australia, the endemic stingless bee Tetragonula carbonaria is widely distributed and known to be an efficient pollinator of both native plants and agricultural crops. In controlled laboratory conditions, we tested the innate colour responses of naïve bees using standard broadband reflectance stimuli representative of common flower colours. Colorimetric analyses considering hymenopteran vision and a hexagon colour space revealed a difference between test colonies, and a significant effect of green contrast and an interaction effect of green contrast with spectral purity on bee choices. We also observed colour preferences for stimuli from the blue and blue-green categorical regions of colour space. Our results are discussed in relation to the similar distribution of flower colours observed from bee pollination around the world.

Distinctive convergence in Australian floral colours seen through the eyes of Australian birds.

We used a colour-space model of avian vision to assess whether a distinctive bird pollination syndrome exists for floral colour among Australian angiosperms. We also used a novel phylogenetically based method to assess whether such a syndrome represents a significant degree of convergent evolution. About half of the 80 species in our sample that attract nectarivorous birds had floral colours in a small, isolated region of colour space characterized by an emphasis on long-wavelength reflection. The distinctiveness of this 'red arm' region was much greater when colours were modelled for violet-sensitive (VS) avian vision than for the ultraviolet-sensitive visual system. Honeyeaters (Meliphagidae) are the dominant avian nectarivores in Australia and have VS vision. Ancestral state reconstructions suggest that 31 lineages evolved into the red arm region, whereas simulations indicate that an average of five or six lineages and a maximum of 22 are likely to have entered in the absence of selection. Thus, significant evolutionary convergence on a distinctive floral colour syndrome for bird pollination has occurred in Australia, although only a subset of bird-pollinated taxa belongs to this syndrome. The visual system of honeyeaters has been the apparent driver of this convergence.

Flower colour and size-signals vary with altitude and resulting climate on the tropical-subtropical islands of Taiwan.

The diversity of flower colours in nature provides quantifiable evidence for how visitations by colour sensing insect pollinators can drive the evolution of angiosperm visual signalling. Recent research shows that both biotic and abiotic factors may influence flower signalling, and that harsher climate conditions may also promote salient signalling to entice scarcer pollinators to visit. In parallel, a more sophisticated appreciation of the visual task foragers face reveals that bees have a complex visual system that uses achromatic vision when moving fast, whilst colour vision requires slower, more careful inspection of targets. Spectra of 714 native flowering species across Taiwan from sea level to mountainous regions 3,300 m above sea level (a.s.l.) were measured. We modelled how the visual system of key bee pollinators process signals, including flower size. By using phylogenetically informed analyses, we observed that at lower altitudes including foothills and submontane landscapes, there is a significant relationship between colour contrast and achromatic signals. Overall, the frequency of flowers with high colour contrast increases with altitude, whilst flower size decreases. The evidence that flower colour signaling becomes increasingly salient in higher altitude conditions supports that abiotic factors influence pollinator foraging in a way that directly influences how flowering plants need to advertise.

Flower reflectance and floral traits data from Ökologisch-Botanischer Garten (OBG), Germany.

Not all colours are perceived and interpreted equally. The electromagnetic spectrum is perceived differently by the distinct visual systems of animal species, resulting in differences in each species' colour perception. Given the diverse colours found in flowering plants, it is interesting to consider the colour perception of insects and the co-evolution of flowering plants to attract pollinators. Here, we considered the differences between human visual systems and that of bees and flies-the two largest insect pollinator groups. We collected flower reflectance spectral data of 73 species across seven human-perceived colours using a spectrophotometer. Minimum of 3 different flowers were used to measure the reflectance properties of flower colours. The raw data can be used to visualize the different animals' visual systems i.e. it can be processed and translated into known photoreceptors of human, bee, and fly visual systems. Overall, our data will help to compare how different animals see flower colours in the natural world and will also highlight the importance of understanding the interspecific communication in plant-pollinator communities. Thus, our data will assist scientists in the future to recognize the floral colour evolution in angiosperms.

Shades of red: bird-pollinated flowers target the specific colour discrimination abilities of avian vision.

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.

Reproductive Isolation Among Three Nocturnal Moth-Pollinated Sympatric Habenaria Species (Orchidaceae).

Comparison and quantification of multiple pre- and post-pollination barriers to interspecific hybridization are important to understand the factors promoting reproductive isolation. Such isolating factors have been studied recently in many flowering plant species which seek after the general roles and relative strengths of different pre- and post-pollination barriers. In this study, we quantified six isolating factors (ecogeographic isolation, phenological isolation, pollinator isolation, pollinia-pistil interactions, fruit production, and seed development) that could possibly be acting as reproductive barriers at different stages among three sympatric Habenaria species (H. limprichtii, H. davidii, and H. delavayi). These three species overlap geographically but occupy different microhabitats varying in soil water content. They were isolated through pollinator interactions both ethologically (pollinator preference) and mechanically (pollinia attachment site), but to a variable degree for different species pairs. Interspecific crosses between H. limprichtii and H. davidii result in high fruit set, and embryo development suggested weak post-pollination barriers, whereas bidirectional crosses of H. delavayi with either of the other two species fail to produce fruits. Our results revealed that pollinators were the most important isolating barrier including both ethological and mechanical mechanisms, to maintain the boundaries among these three sympatric Habenaria species. Our study also highlights the importance of a combination of pre-and post-pollination barriers for species co-existence in Orchidaceae.

Australian native flower colours: Does nectar reward drive bee pollinator flower preferences?

Colour is an important signal that flowering plants use to attract insect pollinators like bees. Previous research in Germany has shown that nectar volume is higher for flower colours that are innately preferred by European bees, suggesting an important link between colour signals, bee preferences and floral rewards. In Australia, flower colour signals have evolved in parallel to the Northern hemisphere to enable easy discrimination and detection by the phylogenetically ancient trichromatic visual system of bees, and native Australian bees also possess similar innate colour preferences to European bees. We measured 59 spectral signatures from flowers present at two preserved native habitats in South Eastern Australia and tested whether there were any significant differences in the frequency of flowers presenting higher nectar rewards depending upon the colour category of the flower signals, as perceived by bees. We also tested if there was a significant correlation between chromatic contrast and the frequency of flowers presenting higher nectar rewards. For the entire sample, and for subsets excluding species in the Asteraceae and Orchidaceae, we found no significant difference among colour categories in the frequency of high nectar reward. This suggests that whilst such relationships between flower colour signals and nectar volume rewards have been observed at a field site in Germany, the effect is likely to be specific at a community level rather than a broad general principle that has resulted in the common signalling of bee flower colours around the world.

Floral Color Diversity: How Are Signals Shaped by Elevational Gradient on the Tropical-Subtropical Mountainous Island of Taiwan?

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 co-existence 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.

Automated calculation of spectral-reflectance marker-points to enable analysis of plant colour-signalling to pollinators.

A spectral reflectance curve for a coloured surface can be constructed from a set of radiation reflectance value measurements made across the spectrum at discrete wavelengths. The curve gives an indication of the pattern of light entering the eye of an organism viewing an illuminated object. Marker points represent the positions along a reflectance curve at which sharp transitions in reflectance occur, these being potentially important to visual perception, for instance by insects discriminating between two flowers, each of a different colour. Consequently, methods of marker point analysis have been applied in several studies evaluating flower colours. These studies have sometimes required researchers to place marker points on reflectance curves by eye, or they have used algorithms written as unreleased software. To automate the process systematically and provide open access, we implemented special-purpose software in C++. Below we provide a summary of the approach adopted in our implementation and made available online in a port to TypeScript. The main benefits of our method are summarized as being:•Automation and repeatability.•Standardisation, cross-platform compatibility and Open Access.•Interactive exploration of the effects of parameter variation.

Fragmentary Blue: Resolving the Rarity Paradox in Flower Colors.

Blue is a favored color of many humans. While blue skies and oceans are a common visual experience, this color is less frequently observed in flowers. We first review how blue has been important in human culture, and thus how our perception of blue has likely influenced the way of scientifically evaluating signals produced in nature, including approaches as disparate as Goethe's Farbenlehre, Linneaus' plant taxonomy, and current studies of plant-pollinator networks. We discuss the fact that most animals, however, have different vision to humans; for example, bee pollinators have trichromatic vision based on UV-, Blue-, and Green-sensitive photoreceptors with innate preferences for predominantly short-wavelength reflecting colors, including what we perceive as blue. The subsequent evolution of blue flowers may be driven by increased competition for pollinators, both because of a harsher environment (as at high altitude) or from high diversity and density of flowering plants (as in nutrient-rich meadows). The adaptive value of blue flowers should also be reinforced by nutrient richness or other factors, abiotic and biotic, that may reduce extra costs of blue-pigments synthesis. We thus provide new perspectives emphasizing that, while humans view blue as a less frequently evolved color in nature, to understand signaling, it is essential to employ models of biologically relevant observers. By doing so, we conclude that short wavelength reflecting blue flowers are indeed frequent in nature when considering the color vision and preferences of bees.

Iridescence and hydrophobicity have no clear delineation that explains flower petal micro-surface.

Plant organs including flowers and leaves typically have a variety of different micro-structures present on the epidermal surface. These structures can produce measurable optical effects with viewing angle including shifts in peak reflectance and intensity; however, these different structures can also modulate hydrophobic properties of the surfaces. For some species optical effects have been proposed to act as signals to enhance pollination interactions, whilst the ability to efficiently shed water provides physiological advantages to plants in terms of gas exchange and reducing infections. Currently, little is known about epidermal surface structure of flowering plants in the Southern Hemisphere, and how micro-surface may be related with either hydrophobicity or visual signalling. We measured four Australian native species and two naturalised species using a combination of techniques including SEM imaging, spectral sampling with a goniometer and contact angle measurements. Spectral data were evaluated in relation to published psychophysics results for important pollinators and reveal that potential visual changes, where present, were unlikely to be perceived by relevant pollinators. Nevertheless, hydrophobicity also did not simply explain petal surfaces as similar structures could in some cases result in very different levels of water repellency.