A new interpretation of flower guide colouration: Absorption of ultraviolet light enhances colour saturation

In melittophilous plants the colour pattern of the flowers, as perceived by bumblebees, is a gradient of centripetally increasing spectral purity. This pattern serves as a signal for innate flower recognition in naive bumblebees permitting orientation to flowers and landing on flowers. Structures which make up the total signal pattern can include the background (e.g., green leaves), corollas, and stamens or floral guides. How various colour parameters, such as dominant wavelength, intensity, and spectral purity influence the colour signal pattern of flowers is analyzed. The process of strong absorption of ultraviolet light is shown to be a mechanism for the enhancement of spectral purity in flower guides. The importance of other mechanisms is also demonstrated. The presence of a gradient of centripetally increasing spectral purity in floral colour patterns as perceived by a bumblebee's eyes is demonstrated by a comparison of the spectral reflectance in different parts of the flower and a representation of colour loci in the colour triangle.     

Unidirectionality of floral colour changes

Many angiosperms have arranged their flowers in inflorescences forming a distinct signalling unit to flower visitors. In some species, the flowers of inflorescences undergo a temporal colour change corresponding exactly to a change in the reward status. Based on information obtained from the spectral reflection curves of pre-change and postchage colours of flower corollas and/or floral guides, it was possible to demonstrate that the colour phase associated with reward closely corresponds to the visual stimuli which trigger behavioural responses of inexperienced flower visitors, and that the colour phase associated with less reward corresponds to visual stimuli less attractive to naïve flower visitors. Reciprocal colour changes were not observed. It is to be assumed that the unidirectionality of floral colour changes is an adaptation of angiosperms aimed at the guidance of first-time flower visitors. Signalling reward to inexperienced flower visitors is an additional function of floral colour changes. The main function of floral colour changes, however, is to provide cues with which the flower visitors can learn to associate one colour phase with reward.     

The effect of polyploidy and hybridization on the evolution of floral colour in Nicotiana (Solanaceae)

Background and Aims Speciation in angiosperms can be accompanied by changes in floral colour that may influence pollinator preference and reproductive isolation. This study investigates whether changes in floral colour can accompany polyploid and homoploid hybridization, important processes in angiosperm evolution.Methods Spectral reflectance of corolla tissue was examined for 60 Nicotiana (Solanaceae) accessions (41 taxa) based on spectral shape (corresponding to pigmentation) as well as bee and hummingbird colour perception in order to assess patterns of floral colour evolution. Polyploid and homoploid hybrid spectra were compared with those of their progenitors to evaluate whether hybridization has resulted in floral colour shifts.Key Results Floral colour categories in Nicotiana seem to have arisen multiple times independently during the evolution of the genus. Most younger polyploids displayed an unexpected floral colour, considering those of their progenitors, in the colour perception of at least one pollinator type, whereas older polyploids tended to resemble one or both of their progenitors.Conclusions Floral colour evolution in Nicotiana is weakly constrained by phylogeny, and colour shifts do occur in association with both polyploid and homoploid hybrid divergence. Transgressive floral colour in N. tabacum has arisen by inheritance of anthocyanin pigmentation from its paternal progenitor while having a plastid phenotype like its maternal progenitor. Potentially, floral colour evolution has been driven by, or resulted in, pollinator shifts. However, those polyploids that are not sympatric (on a regional scale) with their progenitor lineages are typically not divergent in floral colour from them, perhaps because of a lack of competition for pollinators.     

A generalised mimicry system involving angiosperm flower colour, pollen and bumblebees’ innate colour preferences

Flower colour is a major advertisement signal of zoophilous plants for pollinators. Bees, the main pollinators, exhibit innate colour preferences, which have often been attributed to only one single floral colour, though most flowers display a pattern of two or several colours. The existing studies of floral colour patterns are mostly qualitative studies. Using a model of bee colour vision we quantitatively investigate two questions: whether or not component colours of floral colour patterns may mimic pollen signals, and whether or not bumblebees exhibit innate preferences for distinct parameters of naturally existing floral colour patterns. We analysed the spectral reflectances of 162 plant species with multicoloured flowers and inflorescences, distiniguishing between inner and outer colours of floral colour patterns irrespective of the particular structures so coloured.We found that:– The inner colour of radially symmetrical flowers and inflorescences and of zygomorphic flowers appears less diverse to bees than the peripheral colour.– The inner colour of most radial flowers and inflorescences as well as the inner colour of a large number of non-related zygomorphic flowers appears to bees to be very similar to that of pollen.– Bumblebees (Bombus terrestris) exhibit innate preferences for two-coloured over single-coloured dummy flowers in a spontaneous choice test.– Bumblebees exhibit innate preferences for dummy flowers with a large over those with a small centre area.– Bumblebees exhibit innate preferences for dummy flowers with a centre colour similar to that of pollen over those with another centre colour.Our findings support the hypotheses that the inner component of floral colour patterns could be interpreted as a generalised and little recognised form of mimicry of the colour of visually displayed pollen, that bumblebees exhibit innate preferences regarding colour and size parameters of floral colour patterns, and that these correspond to visually displayed pollen. These findings together suggest a prominent role of floral colour patterns in advertisement to and guidance of naive flower visitors.     

Colour choices of naive bumble bees and their implications for colour perception

The innate preferences of inexperienced bumble bees, Bombus terrestris, for floral colour stimuli were studied using artificial flowers. The artificial flowers provided a colour pattern and consisted of a star-shaped corolla and of central colour patches similar to the nectar guide of natural flowers. The innate choice behaviour was assessed in terms of the number of approach flights from some distance towards the artificial flowers and the percentage of approach flights terminating in antennal contact with the floral guide. The colours of the floral guide, the corolla and the background were varied. It was shown that the innate flower colour preference in bumble bees has two components. 1. The frequency of approaches from a distance is correlated with the colour difference between the corolla and the background against which it is presented. If the corolla colour was constant but its background colour varied, the relative attractiveness of the corolla increased with its colour difference to the background. The colour difference assessment underlying this behaviour on a perceptual basis can be attained by means of colour opponent coding, a system well-established in Hymenoptera. 2. The frequency of antennal contacts with the floral guides relative to that of approach flights cannot be accounted for by colour opponent coding alone. Whether the approach flights are interrupted, or whether they end in an antennal contact with the nectar guide is strongly dependent on the direction (sign) of the colour difference, not only its magnitude. The choice behaviour requires a unique perceptual dimension, possibly that of colour saturation or that of hue perception comparable to components of colour perception in humans.     

Innate colour preferences of flower visitors

Freshly emerged flower visitors exhibit colour preferences prior to individual experience with flowers. The understanding of innate colour preferences in flower visitors requires a detailed analysis, as, on the one hand, colour is a multiple-signal stimulus, and, on the other hand, flower visits include a sequence of behavioural reactions each of which can be driven by a preferential behaviour. Behavioural reactions, such as the distant approach, the close-range orientation, the landing, and the extension of mouthparts can be triggered by colour stimuli. The physiological limitations of spectral sensitivity, the neuro-sensory filters, and the animals' different abilities to make use of visual information such as brightness perception, wavelength-specific behaviour and colour vision shape colour preferences. Besides these receiverbased factors, there are restrictions of flower colouration due to sender-based factors such as the absorption properties of floral pigments and the dual function of flower colours triggering both innate and learned behaviour. Recordings of the spectral reflection of coloured objects, which trigger innate colour preferences, provide an objective measure of the colour stimuli. Weighting the spectral reflection of coloured objects by the spectral composition of the ambient light and the spectral sensitivity of the flower visitors' photoreceptors allows the calculation of the effective stimuli. Perceptual dimensions are known for only a few taxa of flower visitors.     

Floral colour versus phylogeny in structuring subalpine flowering communities

The relative number of seeds produced by competing species can influence the community structure; yet, traits that influence seed production, such as pollinator attraction and floral colour, have received little attention in community ecology. Here, we analyse floral colour using reflectance spectra that include near-UV and examined the phylogenetic signal of floral colour. We found that coflowering species within communities tended to be more divergent in floral colour than expected by chance. However, coflowering species were not phylogenetically dispersed, in part due to our finding that floral colour is a labile trait with a weak phylogenetic signal. Furthermore, while we found that locally rare and common species exhibited equivalent floral colour distances from their coflowering neighbours, frequent species (those found in more communities) exhibited higher colour distances from their coflowering neighbours. Our findings support recent studies, which have found that (i) plant lineages exhibit frequent floral colour transitions; and (ii) traits that influence local population dynamics contribute to community structure.     

Anthecology of Orchis mascula (Orchidaceae)

Interactions between Orchis mascula L. ssp. mascula and anthophilous insects were studied mainly on the island of Öland, Sweden. The species is nectarless and acts by deceiving various bees (Hymenoptera, Apoidea). Temporary seeking/exploratory drives of bees for food–sources were exploited by means of superiority in floral display. A floral reflectance maximum at 440 nm (blue) largely determines the colour in the visual spectrum of bees. The floral scent is composed to about 90% of mono–terpenes. Nothing suggested mimesis of concurrent food–flowers either in colour or in scent. Anthesis covered a time period in late spring when (a) concurrent food–flowers for bees were rather few, (b) many bumble–bee queens (Bombus Latr. spp.) were inexperienced as regards food–flowers and had no foraging routines, (c) cuckoo bumble–bee females (Psithyrus Lep. spp.) recovery–fed on flowers after hibernation, (d) males of Eucera longicornis (L.) (Anthophoridae) patrolled far out from their nest–area, and when (e) many solitary bee species flew about. The pollinator fauna differed between sites, viz. either Bombus queens, Psithyrus females or E. longicornis males transported the majority of the pollinaria. The pollination system does not seem to be stabilised in the study areas. Floral morphology indicates that the plant's anthecological specialisation to bees as a group implies a graded unspecialisation to each species of bee in the legitimate pollinator group.     

A bee’s eye view of remarkable floral colour patterns in the south-west Australian biodiversity hotspot revealed by false colour photography

Background and AimsColour 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 advertising of floral traits guides visitation by the insects, ensuring precision in pollen gathering and deposition. The study, focused in the Southwest Australian Floristic Region, aimed to spot bee colour patterns that are usual and unusual, missing, accomplished by mimicry of pollen and anthers, and overlapping between mimic-model species in floral mimicry cases.MethodsFloral colour patterns were examined by false colour photography in 55 flower species of multiple highly diverse natural plant communities in south-west Australia. False colour photography is a method to transform a UV photograph and a colour photograph into a false colour photograph based on the trichromatic vision of bees. This method is particularly effective for rapid screening of large numbers of flowers for the presence of fine-scale bee-sensitive structures and surface roughness that are not detectable using standard spectrophotometry.Key ResultsBee- and bird-pollinated flowers showed the expected but also some remarkable and unusual previously undetected floral colour pattern syndromes. Typical colour patterns include cases of pollen and flower mimicry and UV-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 the orchid genera (Diuris and Thelymitra) that employ floral mimicry of model species, we revealed a surprising mimicry phenomenon of anthers mimicked in turn by model species.ConclusionThe 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.     

The impact of biochemistry vs. population membership on floral scent profiles in colour polymorphic Hesperis matronalis

Background and Aims

Studies of floral scent evolution often attribute variation in floral scent to differences in pollinator behaviour, ignoring the potential for shared biochemistry between floral scent and floral colour to dictate patterns of phenotypic variation in scent production. To determine the relative effects of shared biochemistry and/or localized population-level phenomena on floral scent phenotype, floral scent composition and emission rate were examined in five wild populations of colour polymorphic Hesperis matronalis (Brassicaceae).

Methods

Floral scent was collected by in situ dynamic headspace extraction on purple and white colour morphs in each of five wild populations. Gas chromatography–mass spectroscopy of extracts allowed determination of floral scent composition and emission rate for all individuals, which were examined by non-metric multidimensional scaling and analysis of variance (ANOVA), respectively, to determine the contributions of floral colour and population membership to scent profile variation.

Key Results

Despite the fact that colour morph means were very similar in some populations and quite different in other populations, colour morphs within populations did not differ from each other in terms of scent composition or emission rate. Populations differed significantly from one another in terms of both floral scent composition and emission rate.

Conclusions

Shared biochemistry alone cannot explain the variation in floral scent phenotype found for H. matronalis. Such a result may suggest that the biochemical association between floral scent and floral colour is complex or dependent on genetic background. Floral scent does vary significantly with population membership; several factors, including environmental conditions, founder effects and genetics, may account for this differentiation and should be considered in future studies.Key words: Hesperis matronalis, floral scent, floral colour, plant volatiles, population differentiation, scent composition, scent emission rate, terpenoids, aromatics     

Pollinating birds differ in spectral sensitivity

Pollinating animals and their angiosperm hosts often show strong co-adaptation in traits that increase the likelihood of a successful transfer of pollen and nutrient rewards. One such adaptation is the reported colour difference caused by unequal distribution of anthocyanidin pigments amongst plant species visited by hummingbirds and passerines. This phenomenon has been suggested to reflect possible differences in the colour vision of these pollinating birds. The presence of any such difference in colour vision would arguably affect the ecological and evolutionary interactions between flowers and their visitors, accentuating differences in floral displays and attractiveness of plants to the favoured avian pollinators. We have tested for differences in colour vision, as indicated by the amino acid present at certain key positions in the short-wavelength-sensitive type 1 (SWS1) visual pigment opsin, between the major groups of pollinating birds: the non-passerine Trochilidae (hummingbirds), the passerine Meliphagidae (honeyeaters) and Nectariniidae (sunbirds) plus five other Passerida passerine families. The results reveal gross spectral sensitivity differences between hummingbirds and honeyeaters, on the one hand, and the Passerida species, on the other.     

Pollination of the lady's slipper Cypripedium henryi Rolfe (Orchidaceae)

The pollination ecology of Cypripedium henryi Rolfe, a slipper orchid endemic to west China, was investigated, and its floral shape, size, colour, and scent were analysed. Examination of the breeding system suggests that the flowers are self-compatible, but need pollen vectors for successful reproduction. The flower is rewardless; over 15 insects belonging to Araneida, Hymenoptera, Diptera, Lepidoptera, and Coleoptera were recorded as flower visitors, but most only alighted or rested on the flower. In the total 32 h of observations over 2 years, female Lasioglossum bees were found to be the most frequent visitors and the only pollinators. They showed a high visitation frequency and, surprisingly, re-visited the same flowers frequently. Cypripedium henryi probably attracts pollinators visiting the flowers through general food deception (odour components, colour, false nectar guides), as well as special structures (slippery labellum, slippery staminode). Although three Lasioglossum species visited the flowers, only L. sauterum Fan et Ebmer was found with pollen. Lasioglossum flavohirtum Ebmer was large and climbed out from the entrance. Morphologically, L. sichuanense Fan et Ebmer could be considered as a potential pollinator, but the collected specimens were found to have no pollen of C. henryi on their bodies. It was speculated that the particular floral scent of C. henryi discouraged the entrance of L. sichuanense bees. Lasioglossum sauterum was matched morphologically to the flower, but not all of the visitations resulted in effective pollinations, as some flowers of C. henryi were frequently re-visited and the pollen mass had been taken away by bees on previous visitations. © 2008 The Linnean Society of London, Botanical Journal of the Linnean Society , 2008, 156 , 491–499.     

Floral traits and phenology drive pollinators diversity and pollinators visits in selected endemic Elaeocarpus spp. of the Western Ghats

The detailed studies on phenology, floral morphology in relation to pollination of six endemic species of Elaeocarpus were carried out at different forest areas of Southern Western Ghats, India. The pollinators were attracted by morphology and nature of flowers with different types of rewards offered by the flowers of Elaeocarpus. The number of flowers per tree has determined its type of pollinators, in which, Coleoptera and Diptera visitation was significant and positive relation with increased number of flowers per tree. However, the visitation by Hymenoptera and Lepidoptera were negatively related with flower numbers per tree. The visitation of Diptera was significant and positive relation with number of petal divisions (fringes) of flowers. Also, it has predicted that higher number of petal divisions may act as an optical advertisement to the floral visitors. Like this, the size of the flower was also one of the factors to attract the members Diptera. Also, the size of the flower was negative and significant relation with members of Hymenoptera. Moreover, the visitation of Coleoptera and Lepidoptera were also affected by the size of the flowers. The pollen production was also positive and significant relation with the visitation of Hymenoptera and Coleoptera. Therefore, it may be assumed that the primary reward for Hymenoptera and Coleoptera will be pollen grains.     

Colour association influences honey bee choice between sucrose concentrations

Certain colours associated with floral food resources are more quickly learned by honey bees (Apis mellifera) than are other colours. But the impact of colour, and other floral cues, on bee choice behaviour has not yet been determined. In these experiments, colour association and sugar concentration of reward were varied to assess how they interact to affect bee choice behaviour. Thirty-five bees were individually given binary choices between blue and yellow artificial flowers that contained either the same rewards or rewards of different sucrose concentrations. Honey bee choice between sucrose concentrations was affected by colour association and this effect was greatest when absolute difference between rewards was the lowest. The honey bee's ability to maximize energetic profitability during foraging is constrained by floral cue effectiveness.     

Are pollinators the agents of selection on flower colour and size in irises?

Plant–pollinator interactions are believed to play a major role in the evolution of floral traits. Flower colour and flower size are important for attracting pollinators, directly influencing reproduction, and thus expected to be under pollinator‐mediated selection. Pollinator‐mediated selection is also proposed to play a role in maintaining flower colour polymorphism within populations. However, pigment concentrations, and thus flower colour, are also under selective pressures independent of pollinators. We quantified phenotypic pollinator‐mediated selection on flower colour and size in two colour polymorphic Iris species. Using female fitness, we estimated phenotypic selection on flower colour and size, and tested for pollinator‐mediated selection by comparing selection gradients between flowers open to natural pollination and supplementary pollinated flowers. In both species, we found evidence for pollen limitation, which set the base for pollinator‐mediated selection. In the colour dimorphic Iris lutescens, while pigment concentration and flower size were found to be under selection, this was independent of pollinators. For the polymorphic Iris pumila, pigment concentration is under selective pressure by pollinators, but only for one colour morph. Our results suggest that pollinators are not the main agents of selection on floral traits in these irises, as opposed to the accepted paradigm on floral evolution. This study provides an opposing example to the largely‐accepted theory that pollinators are the major agent of selection on floral traits.     

Phototactic behaviour of the parasitoid Encarsia formosa (Hymenoptera: Aphelinidae)

We investigated the spectral sensitivity and response to light intensity of Encarsia formosa (Hymenoptera: Aphelinidae), which is a key natural enemy of the greenhouse whitefly, Trialeurodes vaporariorum, and the tobacco whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae). To do so, we used 15 monochromatic lights (emitting various specific wavelengths from 340 to 649?nm) and white light. E. formosa adults, which are diurnal insects, showed a positive phototaxis to a broad spectrum of light, with peaks of sensitivity at 414, 340, 450, and 504?nm. These results show that this parasitoid is generally more sensitive to short wavelength lights than long wavelength lights across all spectral ranges tested. Furthermore, E. formosa adults showed an increased phototactic response at low intensities and a decreased response at high intensities, for both ultraviolet light and violet light. Thus, E. formosa showed both colour and intensity preferences. This experiment provides a scientific basis for the development of colour traps for insect pest management and improves understanding of the ecological significance of colour vision by E. formosa.     

Monitoring bee populations: are eusocial bees attracted to different colours of pan trap than other bees?

Declines in pollinator populations have made monitoring pollinators, in particular bees, increasingly important. There is general agreement among practitioners that using a mix of trap colours is important, but the empirical evidence to support this is scattered. During studies of bees in forestry cutovers, large differences were noted in capture rate among white, blue, and yellow pan traps. Pooled data from collections in cutovers and commercial cranberry fields demonstrated significant differences in the effect of trap colour, with the largest numbers captured in white traps, and the fewest in yellow, but only for the genus Bombus Latreille (Hymenoptera: Apidae). The colour preference was consistent with the spectral sensitivity of Bombus, and the visible reflectance spectra of the traps. A literature review suggested that among eusocial bees, Apis Linnaeus (Hymenoptera: Apidae) are more attracted to white traps and Bombus are more attracted to blue traps, while non-eusocial bees with a variety of social structures are more attracted to yellow. Among the non-eusocial bees, Halictidae were somewhat attracted to blue, while Andrenidae were not. This supports the common practice of using white, blue, and yellow traps when surveying bees to ensure adequate taxonomic representation.     

Floral trait differentiation in Anacamptis coriophora: Phenotypic selection on scents,but not on colour

Current divergent selection may promote floral trait differentiation among conspecific populations in flowering plants. However, whether this applies to complex traits such as colour or scents has been little studied, even though these traits often vary within species. In this study, we compared floral colour and odour as well as selective pressures imposed upon these traits among seven populations belonging to three subspecies of the widespread, generalist orchid Anacamptis coriophora. Colour was characterized using calibrated photographs, and scents were sampled using dynamic headspace extraction and analysed using gas chromatography–mass spectrometry. We then quantified phenotypic selection exerted on these traits by regressing fruit set values on floral trait values. We showed that the three studied subspecies were characterized by different floral colour and odour, with one of the two predominant floral volatiles emitted by each subspecies being taxon‐specific. Plant size was positively correlated with fruit set in most populations, whereas we found no apparent link between floral colour and female reproductive success. We detected positive selection on several taxon‐specific compounds in A. coriophora subsp. fragrans, whereas no selection was found on floral volatiles of A. coriophora subsp. coriophora and A. coriophora subsp. martrinii. This study is one of the first to document variation in phenotypic selection exerted on floral scents among conspecific populations. Our results suggest that selection could contribute to ongoing chemical divergence among A. coriophora subspecies.     

Insect preference for symmetrical artificial flowers

An insect preference for floral symmetry may be maintained because plants with symmetrical flowers, which are able to control developmental processes under given environmental conditions, also are able to provide more pollinator rewards than plants with asymmetrical flowers. Alternatively, insects may have an inherent preference for symmetrical structures and thereby impose selection for the maintenance of symmetry in flowers even in the absence of any pollinator rewards. We tested for an insect preference for radially symmetrical flowers by using horizontally placed units of four circular coloured flower models varying in size and symmetry. The shape and colour of the model flowers did not resemble any naturally occurring flowers in the environment. Insects and Hymenoptera, respectively (five species of Diptera and one species of Coleoptera) that visited the flower models clearly preferred symmetrical models over asymmetrical ones, and the ranking of visits to the models reflected a preference for large, symmetrical flowers. These results provide evidence for a preference for symmetrical flower models, even in the absence of pollinator rewards. Received: 11 September 1997 / Accepted: 2 November 1997     

Butterflies show flower colour preferences but not constancy in foraging at four plant species

1. The extent to which flower colour and other visual cues influence butterfly flower choice in the field is poorly understood, especially in comparison with choices by Hymenoptera. 2. Using a novel approach to studies of visitation behaviour by butterflies, flower colour of four Asteraceae species was phenotypically manipulated to decouple the influence of that trait from others (including morphology and nectar rewards) on visitation by Lycaena heteronea, Speyeria mormonia, Cercyonis oetus, and Phyciodes campestris. 3. Flower visits were recorded to experimental flower arrays in subalpine meadows to measure (i) spontaneous preference by butterflies for particular colours and other traits and (ii) flower constancy (longer than expected strings of visits made to flowers of the same species), a behaviour that can reduce interspecific gene flow in plants. 4. Over three field seasons, 3558 individual flower visits in 1386 foraging bouts were observed for free‐flying butterflies. All four butterfly species responded to the phenotypic manipulations of flower colour, although in different ways. Speyeria mormonia and L. heteronea also exhibited preferences based on other flower traits. Lycaena heteronea responded to combinations of traits such that the other traits it preferred depended upon the context of flower colour. 5. None of the butterfly species exhibited flower constancy in any of the arrays employed. 6. The observed preferences show that butterflies, like some other pollinators, are potentially capable of exerting selection on colour and other floral traits. Moreover, these flower preferences can depend on the context of other flower traits. The absence of constancy contrasts with reports of high constancy in many bees.