Bee-pollinated Flowers Research Articles

Genetic basis of nectar guide trichome variation between bumblebee- and self-pollinated monkeyflowers (Mimulus): role of the MIXTA-like gene GUIDELESS

Nectar guide trichomes play crucial ecological roles in bee-pollinated flowers, as they serve as footholds and guides for foraging bees to access the floral rewards. However, the genetic basis of natural variation in nectar guide trichomes among species remains poorly understood. In this study, we performed genetic analysis of nectar guide trichome variation between two closely related monkeyflower (Mimulus) species, the bumblebee-pollinated Mimulus lewisii and self-pollinated M. parishii. We demonstrate that a MIXTA-like R2R3-MYB gene, GUIDELESS, is a major contributor to the nectar guide trichome length variation between the two species. The short-haired M. parishii carries a recessive allele due to non-synonymous substitutions in a highly conserved motif among MIXTA-like MYB proteins. Furthermore, our results suggest that besides GUIDELESS, additional loci encoding repressors of trichome elongation also contribute to the transition from bumblebee-pollination to selfing. Taken together, these results suggest that during a pollination syndrome switch, changes in seemingly complex traits such as nectar guide trichomes could have a relatively simple genetic basis, involving just a few genes of large effects.

Ecological Diversification in an Adaptive Radiation of Plants: The Role of De Novo Mutation and Introgression.

Adaptive radiations are characterized by rapid ecological diversification and speciation events, leading to fuzzy species boundaries between ecologically differentiated species. Adaptive radiations are therefore key systems for understanding how species are formed and maintained, including the role of de novo mutations versus preexisting variation in ecological adaptation and the genome-wide consequences of hybridization events. For example, adaptive introgression, where beneficial alleles are transferred between lineages through hybridization, may fuel diversification in adaptive radiations and facilitate adaptation to new environments. In this study, we employed whole-genome resequencing data to investigate the evolutionary origin of hummingbird-pollinated flowers and to characterize genome-wide patterns of phylogenetic discordance and introgression in Penstemon subgenus Dasanthera, a small and diverse adaptive radiation of plants. We found that magenta hummingbird-adapted flowers have apparently evolved twice from ancestral blue-violet bee-pollinated flowers within this radiation. These shifts in flower color are accompanied by a variety of inactivating mutations to a key anthocyanin pathway enzyme, suggesting that independent de novo loss-of-function mutations underlie the parallel evolution of this trait. Although patterns of introgression and phylogenetic discordance were heterogenous across the genome, a strong effect of gene density suggests that, in general, natural selection opposes introgression and maintains genetic differentiation in gene-rich genomic regions. Our results highlight the importance of both de novo mutation and introgression as sources of evolutionary change and indicate a role for de novo mutation in driving parallel evolution in adaptive radiations.

Visual function of red staminal filaments in a bee-pollinated plant

ABSTRACT Background Floral colour is a primary signal in plant-pollinator interactions. Presumably because bees lack red receptors, bee-pollinated flowers are rarely red. Hypericum (Hypericaceae) is a genus, with yellow flowers and filaments, mainly pollinated by bees. However, one species, H. ascyron exhibits unique red filaments. Aims We tested whether the red filaments influence pollinator visitation frequency and colour perception. Methods We examined whether H. ascyron require pollinators for seed set and compared insect visitation rates of H. ascyron with those of a sympatric yellow-filamented congener. Colour perception by bees was also estimated. Results Pollinator visitation substantially enhanced seed set under natural conditions and flowers of H. ascyron had similar rates of visitation by bees as their yellow-filamented congener. Red filaments per se absorbed ultraviolet light and therefore should not be perceived as a chromatic colour by bees. The chromatic contrasts between filaments and petals as perceived by pollinators was similar between species, whereas achromatic contrasts were higher in H. ascyron. Conclusions Pure-red staminal filaments work as well in attracting potential pollinators as the yellow filaments of congeners. Based on our findings, we suggest that the evolution of red filament colour may have been driven by factors other than pollinator attraction.

Evolutionary history and climate conditions constrain the flower colours of woody plants in China

AbstractIn this study, we investigated (i) the differences in flower colour composition among growth forms of woody plants in China and (ii) the influences of biogeographic regions, evolutionary age and climatic conditions on geographic variation in the proportions of different flower colours. Using distribution maps and flower colour information (white, red, yellow, yellow-green, green and blue-purple) of 7673 Chinese woody plant species and a dated genus-level phylogenetic tree, we compared flower colour composition among different growth forms (shrubs, trees and lianas). We further estimated the relationships of geographical patterns in the proportions of different flower colours with seven different biogeographic regions, evolutionary age and different contemporary climatic variables. Compared with trees or lianas, shrubs showed a higher proportion of species with anthocyanin-based red and blue-purple flowers. The geographic patterns of flower colour composition of woody plants in China were strongly influenced by regional effects and contemporary climate, especially precipitation and ultraviolet B irradiance. The proportion of species with presumably bee-pollinated yellow and blue-purple flowers and stress tolerant anthocyanin-based red and blue-purple flower colours tended to be high in the northwestern part of China. Green flowers tended to evolve earlier than others, but evolutionary age had quite weak influences on the geographic pattern of flower colours. Our results reflect both evolutionary and environmental constraints on the distribution of flower colours of woody plants in China.

Meaningful Words in Crowd Noise: Searching for Volatiles Relevant to Carpenter Bees among the Diverse Scent Blends of Bee Flowers.

Olfactory cues constitute one of the most important plant-pollinator communication channels. Specific chemical components can be associated with specific pollinator functional groups due to pollinator-mediated selection on flower volatile (FV) emission. Here, we used multivariate analyses of FV data to detect an association between FVs and the worldwide distributed pollinator group of the carpenter bees (Xylocopa spp.). We compiled FVs of 29 plant species: 9 pollinated by carpenter bees, 20 pollinated by other bee pollinator functional groups. We tested whether FV emission differed between these groups. To rule out any phylogenetic bias in our dataset, we tested FV emission for phylogenetic signal. Finally, using field assays, we tested the attractive function of two FVs found to be associated with carpenter bees. We found no significant multivariate difference between the two plant groups FVs. However, seven FVs (five apocarotenoid terpenoids, one long-chain alkane and one benzenoid) were significantly associated with carpenter bee pollination, thus being "predictor" compounds of pollination by this pollinator functional group. From those, β-ionone and (E)-methyl cinnamate presented the highest indicator values and had their behavioural function assessed in field assays. Phylogenetic signal for FVs emission was weak, suggesting that their emission could result from pollinator-mediated selection. In field assays, the apocarotenoid β-ionone attracted carpenter bees, but also bees from other functional groups. The benzenoid (E)-methyl cinnamate did not attract significant numbers of pollinators. Thus, β-ionone functions as a non-specific bee attractant, while apocarotenoid FVs emerge as consistent indicators of pollination by large food-foraging bees among bee-pollinated flowers.

Birds Perceive More Intraspecific Color Variation in Bird-Pollinated Than Bee-Pollinated Flowers.

Pollinator-mediated selection is expected to constrain floral color variation within plant populations. Here, we test for patterns of constraint on floral color variation in 38 bee- and/or hummingbird-pollinated plant species from Colorado, United States. We collected reflectance spectra for at least 15 individuals in each of 1–3 populations of each species (total 78 populations) and modeled perceived color variation in both bee and bird visual spaces. We hypothesized that bees would perceive less intraspecific color variation in bee-pollinated species (vs. bird-pollinated species), and reciprocally, birds would perceive less color variation in bird-pollinated species (vs. bee-pollinated species). In keeping with the higher dimensionality of the bird visual system, birds typically perceived much more color variation than bees, regardless of plant pollination system. Contrary to our hypothesis, bees perceived equal color variation within plant species from the two pollination systems, and birds perceived more color variation in species that they pollinate than in bee-pollinated species. We propose hypotheses to account for the results, including reduced long-wavelength sensitivity in bees (vs. birds), and the ideas that potential categorical color vision in birds and larger cognitive capacities of birds (vs. bees) reduces their potential discrimination against floral color variants in species that they pollinate, resulting in less stabilizing selection on color within bird-pollinated vs. bee-pollinated species.

Intrafloral Color Modularity in a Bee-Pollinated Orchid.

Flower color has been studied in different ecological levels of organization, from individuals to communities. However, it is unclear how color is structured at the intrafloral level. In bee-pollinated flowers, the unidirectional gradient in color purity and pollen mimicry are two common processes to explain intrafloral color patterns. Considering that floral traits are often integrated, usually reflecting evolutionary modules under pollinator-mediated selection, we hypothesize that such intrafloral color patterns are structured by intrafloral color modules as perceived by bee color vision system. Here, we studied the tropical bee-pollinated orchid Cattleya walkeriana, given its intrafloral color complexity and variation among individuals. Considering bee color vision, we investigated if intrafloral color modules arose among intrafloral patches (tip or base of the sepals, petals, and labellum). We expected a separate color module between the labellum patches (the main attractive structure in orchids) and petals and sepals. We measured the color reflectance and calculated the photoreceptor excitation, spectral purity, hue, and the chromatic contrast of the floral structures in the hexagon color model. Spectral purity (saturation) was higher in the labellum tip in comparison to petals and sepals, generating a unidirectional gradient. Labellum base presented a less saturated yellow UV-absorbing color, which may reflect a pollen mimicry strategy. C. walkeriana presented three intrafloral color modules corresponding to the color of petals and sepals, the color of the labellum tip, and the color of labellum base. These color modules were unrelated to the development of floral structures. Given the importance of intrafloral color patterns in bee attraction and guidance, our results suggest that intrafloral patterns could be the outcome of evolutionary color modularization under pollinator-mediated selection.

Honey bees are important pollinators of South African blueberries despite their inability to sonicate

Animal-mediated pollination is an essential ecosystem service on which over a third of the world's agricultural crops depend. Blueberry fruit production is highly dependent on animal pollination and although visited by a range of bee species in their native range and agricultural settings, bumble bees are thought to be their primary native pollinators. Demand for blueberries has increased in recent years due to their perceived health benefits. Consequently, blueberry cultivation has expanded well beyond their native and original agricultural range, including several regions where bumble bees are not present. In South Africa, like many areas in the world, honey bees are the only commercially available pollinators for blueberries because many countries ban the importation of bumble bees. This study aimed to determine the benefits of honey bee pollination on blueberry fruit yield for the variety Ventura by comparing yields of honey bee-pollinated flowers to flowers where pollinators were excluded. Our results show that honey bees significantly increased berry mass and diameter. We conclude that Ventura in South Africa can be pollinated by honey bees, and that honey bee pollination can be an effective substitute for bumble bees in areas where bumble bees are unavailable. We also determined the extent to which blueberry yields could be improved by comparing fruit yield under honey bee pollination to fruit yield achieved through hand pollination. We found that honey bee pollinated blueberry yields were lower than yields achieved through hand pollination, suggesting that there is potentially room to improve honey bee pollination. Furthermore, we offer a conceptual figure to demonstrate how yield obtained through pollinator exclusion, open pollination, and hand pollination relate to each other. Additional research is required to study how beneficial honey bees are to fruit yield on other blueberry varieties as the benefits of honey bees are likely to vary depending on the variety.

Colour evolution within orchids depends on whether the pollinator is a bee or a fly.

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 characterise 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.

How flower colour signals allure bees and hummingbirds: a community-level test of the bee avoidance hypothesis.

Colour signals are the main floral trait for plant-pollinator communication. Owing to visual specificities, flower visitors exert different selective pressures on flower colour signals of plant communities. Although they evolved to attract pollinators, matching their visual sensitivity and colour preferences, floral signals may also evolve to avoid less efficient pollinators and antagonistic flower visitors. We evaluated evidence for the bee avoidance hypothesis in a Neotropical community pollinated mainly by bees and hummingbirds, the campo rupestre. We analysed flower reflectance spectra, compared colour variables of bee-pollinated flowers (bee-flowers; 244 species) and hummingbird-pollinated flowers (hummingbird-flowers; 39 species), and looked for evidence of bee sensorial exclusion in hummingbird-flowers. Flowers were equally contrasting for hummingbirds. Hummingbird-flowers were less conspicuous to bees, reflecting mainly long wavelengths and avoiding red-blind visitors. Bee-flowers reflected more short wavelengths, were more conspicuous to bees (higher contrasts and spectral purity) than hummingbird-flowers and displayed floral guides more frequently, favouring flower attractiveness, discrimination and handling by bees. Along with no phylogenetic signal, the differences in colour signal strategies between bee- and hummingbird-flowers are the first evidence of the bee avoidance hypothesis at a community level and reinforce the role of pollinators as a selective pressure driving flower colour diversity.

Pollination efficiency of artificial and bee pollination practices in kiwifruit

The area cultivated with pollinator-dependent crops is increasing worldwide, while a shortfall in pollinator availability is a growing problem in many agroecosystems. For this reason, many highly pollinator-dependent crops are nowadays pollinated artificially by humans. Here, we compared the efficiency of artificial and bee pollination practices on the mean level and stability of pollination and fruit production of kiwifruit. In a kiwifruit orchard, we tagged a total of 800 flowers from 40 plants, half were pollinated by honeybees while the other half by spraying pollen on flowers, the most commonly pollination technique used in kiwifruit. During harvest, we measured fruit set, number of seeds per fruit, and fruit weight. On average, bee-pollinated plants produced 40% more fruits than artificially-pollinated plants. Also, fruits from bee-pollinated flowers contained, on average, 34% more seeds, showing also 2.8 times less variability in number of seeds per fruit than those pollinated artificially. Following the same trend, bee-pollinated flowers produce fruits that were 34% heavier and 1.5 times less variable in weight. These results showed that bee pollination resulted in higher fruit production, and heavier and more homogeneous fruits than artificial pollination. According to these results, we encourage growers and land managers to use pollination management practices based on honey bees, instead of the use of mechanical pollination systems.

Intraspecific variation in the petal epidermal cell morphology of Vicia faba L. (Fabaceae)

At a microscopic scale, the shape and fine cell relief of the petal epidermal cells of a flower play a key role in its interaction with pollinators. In particular, conical shaped petal epidermal cells have been shown to have an important function in providing grip on the surface of bee-pollinated flowers and can influence bee visitation rates. Previous studies have explored interspecific variation in this trait within genera and families, but naturally-occurring intraspecific variation has not yet been comprehensively studied. Here, we investigate petal epidermal cell morphology in 32 genotypes of the crop Vicia faba, which has a yield highly dependent on pollinators. We hypothesise that conical cells may have been lost in some genotypes as a consequence of selective sweeps or genetic drift during breeding programmes. We find that 13% of our lines have a distribution of conical petal epidermal cells that deviates from that normally seen in V. faba flowers. These abnormal phenotypes were specific to the ad/abaxial side of petals, suggesting that these changes are the result of altered gene expression patterns rather than loss of gene function.

Floral visits of the wild bee, <i>Lithurgus atratus</i>, impact yield and seed germinability of okra, <i>Abelmoschus esculentus</i>, in Sri Lanka

Bee-pollinated crops in landscapes with a low abundance of bees suffer from insufficient pollination. The present study investigates the effect of wild bee pollination on fruit and seed production in okra, Abelmoschus esculentus (L.) Moench. The study was conducted in a home garden, where an okra field was established for three pollination trials each to include 40 okra plants. For each trial, three sets of 25 flower buds were selected and tagged. One set was covered to deter bees, another set was kept open to enable bee visits and the other set was cross-pollinated by hand. Of the two species of bees, Tetragonula iridipennis (Smith) visited flowers for nectar while Lithurgus atratus Smith collected and carried pollen grains. The period of stigma receptivity and pollen availability coincided with the highest activity of L. atratus from 10.00 a.m. to 12.20 p.m. Bee-pollinated flowers had significantly enhanced okra pod length and diameter, seed number and seed germinability compared to the trial with flowers covered to deter bees. Hand pollinated flowers also produced significantly longer pods and a higher number of seeds with higher germinability. Although there was no significant difference in pod length and diameter and seed number between hand pollination trial and bee-pollinated trial, germinability of bee-pollinated seeds was significantly higher. Present study highlights the importance of the wild bee, L. atratus to enhance pod size, seed number and seed germinability in okra in Kurunegala, Sri Lanka.

More than euglossines: the diverse pollinators and floral scents of Zygopetalinae orchids.

Floral volatile organic compounds (VOCs) play important roles in plant-pollinator interactions. We investigated the reproductive ecology and floral VOCs of Zygopetalinae orchids to understand the relationship between floral scents and pollinators. We performed focal observations, phenological censuses and breeding system experiments in eight species in southeast Brazil. Floral scents were collected and analysed using SPME/GC-MS. We performed multivariate analyses to group species according to affinities of their VOCs and define compounds associated to each plant. Dichaea cogniauxiana was pollinated by weevils which use their developing ovules, while D. pendula was pollinated by the same weevils and perfume-collecting male euglossine bees. The other species were deceit-pollinated by bees. Zygopetalum crinitum was pollinated by carpenter bees, while W. warreana, Z. mackayi and Z. maxillare were bumblebee-pollinated. The latter was also pollinated by Centris confusa. Breeding system varied widely with no association to any pollinator group. Most VOCs are common to other floral scents. Zygopetalum crinitum presented an exclusive blend of VOCs, mainly composed of benzenoids. The scents of Pabstia jugosa, Promenaea xanthina and the Zygopetalum spp. were similar. The bumblebee-pollinated species have flowering periods partially overlapped, thus neither phenology nor pollinators constitute hybridization barriers among these species. Euglossines are not the only pollinators of Zygopetalinae. Different VOCs, size and lifespan of flowers are associated with distinct pollinators. A distinctive VOC bouquet may determine specialisation in carpenter bees or male euglossines within bee-pollinated flowers. Finally, visitation of deceit-pollinated flowers by perfume-collecting euglossines allows us to hypothesise how pollination by this group of bees had evolved.

Herbivory as an important selective force in the evolution of floral traits and pollinator shifts.

Floral trait evolution is frequently attributed to pollinator-mediated selection but herbivores can play a key role in shaping plant reproductive biology. Here we examine the role of florivores in driving floral trait evolution and pollinator shifts in a recently radiated clade of flowering plants, Oenothera sect. Calylophus We compare florivory by a specialist, internal feeder, Mompha, on closely related hawkmoth- and bee-pollinated species and document variation in damage based on floral traits within sites, species and among species. Our results show that flowers with longer floral tubes and decreased floral flare have increased Mompha damage. Bee-pollinated flowers, which have substantially smaller floral tubes, experience on average 13% less Mompha florivory than do hawkmoth-pollinated flowers. The positive association between tube length and Mompha damage is evident even within sites of some species, suggesting that Mompha can drive trait differentiation at microevolutionary scales. Given that there are at least two independent shifts from hawkmoth to bee pollination in this clade, florivore-mediated selection on floral traits may have played an important role in facilitating morphological changes associated with transitions from hawkmoth to bee pollination.

Assessing the ecological significance of bee visual detection and colour discrimination on the evolution of flower colours

Bee pollinators interact with flowers in a complex signal-receiver system. Chromatic traits that allow reliable discrimination between rewarding and non-rewarding flowers have been proposed as an important feature of pollination syndromes: bee-pollinated flowers have spectral profiles that closely match the discrimination peaks of their pollinators across the visual spectrum. However, in the complexity of a natural environment, it may be hard for bees to even detect the presence of flowers. In particular, little is known about how discrimination and detection by bees may together contribute to pollinator-mediated selection on floral colour signals. We address here an unexplained feature of floral colour evolution: the extreme paucity of spectral patterns with pronounced changes in reflectance around 420–480 nm wavelength. We began by conducting experiments with honeybees in a Y-maze to determine their capacity to detect a stimulus rarely found in bee-pollinated flowers—one with a single sharp spectral reflectance change at 478 nm. We found bees to be poor at detecting this stimulus against a neutral background. We then conducted behaviourally-informed computer simulations that test how bee visual discrimination and detection interact, which yielded information about which flower colours most effectively facilitate cross-pollination. Finally, we identified from our previous work those bird-pollinated species whose floral colours had spectral characteristics similar to the stimulus used in the Y-maze experiment. These data demonstrate that plants can, and do, produce such spectra for pollinators other than bees. In combination, our results show that the interaction between colour discrimination and detection is important for understanding flower community assembly.

Floral specialization for different pollinators and divergent use of the same pollinator among co-occurringImpatiensspecies (Balsaminaceae) from Southeast Asia

Floral variation among closely related species is thought to often reflect differences in pollination systems. Flowers of the large genus Impatiens are characterized by extensive variation in colour, shape and size and in anther and stigma positioning, but studies of their pollination ecology are scarce and most lack a comparative context. Consequently, the function of floral diversity in Impatiens remains enigmatic. This study documents floral variation and pollination of seven co-occurring Impatiens spp. in the Southeast Asian diversity hotspot. To assess whether floral trait variation reflects specialization for different pollination systems, we tested whether species depend on pollinators for reproduction, identified animals that visit flowers, determined whether these visitors play a role in pollination and quantified and compared key floral traits, including floral dimensions and nectar characteristics. Experimental exclusion of insects decreased fruit and seed set significantly for all species except I. muscicola, which also received almost no visits from animals. Most species received visits from several animals, including bees, birds, butterflies and hawkmoths, only a subset of which were effective pollinators. Impatiens psittacina, I. kerriae, I. racemosa and I. daraneenae were pollinated by bees, primarily Bombus haemorrhoidalis. Impatiens chiangdaoensis and I. santisukii had bimodal pollination systems which combined bee and lepidopteran pollination. Floral traits differed significantly among species with different pollination systems. Autogamous flowers were small and spurless, and did not produce nectar; bee-pollinated flowers had short spurs and large floral chambers with a wide entrance; and bimodally bee- and lepidopteran-pollinated species had long spurs and a small floral chamber with a narrow entrance. Nectar-producing species with different pollination systems did not differ in nectar volume and sugar concentration. Despite the high frequency of bee pollination in co-occurring species, individuals with a morphology suggestive of hybrid origin were rare. Variation in floral architecture, including various forms of corolla asymmetry, facilitates distinct, species-specific pollen-placement on visiting bees. Our results show that floral morphological diversity among Impatiens spp. is associated with both differences in functional pollinator groups and divergent use of the same pollinator. Non-homologous mechanisms of floral asymmetry are consistent with repeated independent evolution, suggesting that competitive interactions among species with the same pollination system have been an important driver of floral variation among Impatiens spp.

Bees, birds and yellow flowers: pollinator-dependent convergent evolution of UV patterns.

Colour is one of the most obvious advertisements of flowers, and occurs in a huge diversity among the angiosperms. Flower colour is responsible for attraction from a distance, whereas contrasting colour patterns within flowers aid orientation of flower visitors after approaching the flowers. Due to the striking differences in colour vision systems and neural processing across animal taxa, flower colours evoke specific behavioural responses by different flower visitors. We tested whether and how yellow flowers differ in their spectral reflectance depending on the main pollinator. We focused on bees and birds and examined whether the presence or absence of the widespread UV reflectance pattern of yellow flowers predicts the main pollinator. Most bee-pollinated flowers displayed a pattern with UV-absorbing centres and UV-reflecting peripheries, whereas the majority of bird-pollinated flowers are entirely UV- absorbing. In choice experiments we found that bees did not show consistent preferences for any colour or pattern types. However, all tested bee species made their first antennal contact preferably at the UV-absorbing area of the artificial flower, irrespective of its spatial position within the flower. The appearance of UV patterns within flowers is the main difference in spectral reflectance between yellow bee- and bird-pollinated flowers, and affects the foraging behaviour of flower visitors. The results support the hypothesis that flower colours and the visual capabilities of their efficient pollinators are adapted to each other.

Gloss, colour and grip: multifunctional epidermal cell shapes in bee- and bird-pollinated flowers.

Flowers bear the function of filters supporting the attraction of pollinators as well as the deterrence of floral antagonists. The effect of epidermal cell shape on the visual display and tactile properties of flowers has been evaluated only recently. In this study we quantitatively measured epidermal cell shape, gloss and spectral reflectance of flowers pollinated by either bees or birds testing three hypotheses: The first two hypotheses imply that bee-pollinated flowers might benefit from rough surfaces on visually-active parts produced by conical epidermal cells, as they may enhance the colour signal of flowers as well as the grip on flowers for bees. In contrast, bird-pollinated flowers might benefit from flat surfaces produced by flat epidermal cells, by avoiding frequent visitation from non-pollinating bees due to a reduced colour signal, as birds do not rely on specific colour parameters while foraging. Moreover, flat petal surfaces in bird-pollinated flowers may hamper grip for bees that do not touch anthers and stigmas while consuming nectar and thus, are considered as nectar thieves. Beside this, the third hypothesis implies that those flower parts which are vulnerable to nectar robbing of bee- as well as bird-pollinated flowers benefit from flat epidermal cells, hampering grip for nectar robbing bees. Our comparative data show in fact that conical epidermal cells are restricted to visually-active parts of bee-pollinated flowers, whereas robbing-sensitive parts of bee-pollinated as well as the entire floral surface of bird-pollinated flowers possess on average flat epidermal cells. However, direct correlations between epidermal cell shape and colour parameters have not been found. Our results together with published experimental studies show that epidermal cell shape as a largely neglected flower trait might act as an important feature in pollinator attraction and avoidance of antagonists, and thus may contribute to the partitioning of flower-visitors.

Generalized pollination system: Are floral traits adapted to different pollinators?

Flowers that are pollinated both during the day and at night could exhibit two different groups of pollinators and produce two different sets of attractants and rewards. We explored the patterns of emission of flower scents and production of nectar in the cactus Echinopsis chiloensis ssp. chiloensis, in relation to the patterns of activity of its diurnal and nocturnal pollinators. We measured frequency of flower visitors, analyzed floral scents, measured nectar production and sugar concentration, and performed pollination exclusion experiments. Bees were the main visitors at daytime and hawkmoths at nighttime. Diurnal scents were dominated by several compounds that can attract a wide range of pollinators, whereas nocturnal scents were less diverse and were dominated by (E)-nerolidol, a compound eliciting antennal responses in hawkmoths. Nectar volume and sugar concentration at night were similar to those recorded in hawkmoth-pollinated flowers. Daytime nectar volume was higher than those commonly found in bee-pollinated flowers, but similar to those found in flowers pollinated by several pollinators. Daytime sugar concentration was similar to those recorded in bee-pollinated flowers. Flowers of E. chiloensis ssp. chiloensis seem morphologically adapted to hawkmoth pollination, but diurnal and nocturnal pollinators contribute to similar extents to reproductive success. Additionally, diurnal and nocturnal pollinators showed a synergic effect on the product of fruit set and seed set. The results are discussed in terms of the linkage between floral traits and perception abilities and requirements of pollinators.