Summary 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.
Summary Floral colour mediates plant–pollinator interactions by often signalling floral resources. In this sense, hummingbird‐pollinated flowers are frequently red‐coloured, and there are two tentative hypotheses to explain this pattern: 1. hummingbirds are attracted to red due its easier detection and 2. bees are sensorially excluded from red flowers. The second hypothesis is based on bees’ red colour blindness, which lead them to be less frequent and less important than hummingbirds as pollinators of red‐reflecting flowers. Here, we untangled the role of different flower traits mediating plant–pollinator interactions and empirically tested the above hypotheses. We chose Costus arabicus due to its synchronopatric white‐ and pink‐flowered individuals and its bee and hummingbird pollination system. Although pink flowers are not totally achromatic as pure red ones, they show an achromaticity degree that could drive bee exclusion. Specifically, we tested whether differences on red reflectance work attracting hummingbirds or excluding bees and the consequent implications for the plant's reproduction. Flower colour morphs of C. arabicus do differ neither in morphology nor in nectar sugar content. Moreover, white and pink flowers can be discriminated by the bees’ and hummingbirds’ colour vision system. Both groups are able to discriminate the red colour variation morph on the flower petals, the white flowers being more easily detected by bees and the pink flowers by hummingbirds. Bees preferentially visited the white flowers, whereas hummingbirds visited both colours at the same rate – both patterns corroborating the second hypothesis. Pollen loads deposited on stigmas did not differ between flower colour morphs, indicating that bees and hummingbirds play a similar role in the overall pollen deposition. However, bees are more likely to self‐pollinate than hummingbirds. Self‐pollination limits C. arabicus reproduction, and red‐reflecting flowers may be better pollinated by discouraging bee visitation. Therefore, the intraspecific colour variation is driving flowers to show colour‐related different levels of generalization. Our results support the ‘bee avoidance’ rather than the ‘hummingbird preference’ hypothesis. Sensory exclusion of bees seems to be the pressure for red‐reflecting flowers evolution, driving specialization in hummingbird‐pollinated flowers due to the costs of bee pollination on plant reproduction.
Angiosperms display an enormous diversity of forms, functions and strategies when it comes to reproduction. This multiplicity has been translated into several terminological concepts and contexts, which have facilitated further research. On the other hand, the use of terms that address the reproduction of flowering plants has been shown to be inconsistent in the literature, complicating communication among specialists. Key terms, such as "reproductive system", "mating system" and "sexual system", among others, have been frequently cited as synonyms, and even used in different circumstances. This review proposes to establish a consistent nomenclatural classification in the field of angiosperms reproductive biology in order to facilitate communication among researchers. Specific terms related to angiosperm reproduction are conceptualized and distributed into five general systems: four related to sexual reproduction (sexual, floral, incompatibility and mating systems); and one related to asexual reproduction (apomictic systems). Our proposal is not to establish a natural classification, but rather to provide a general overview of the main concepts that were grouped here in an artificial and functional manner. Our aim is to advance the field of reproductive biology of angiosperms with consistent and well-defined applications of relevant terminologies.
Flowering and fruiting are key events in the life history of plants, and both are critical to their reproductive success. Besides the role of evolutionary history, plant reproductive phenology is regulated by abiotic factors and shaped by biotic interactions with pollinators and seed dispersers. In Melastomataceae, a dominant Neotropical family, the reproductive systems vary from allogamous with biotic pollination to apomictic, and seed dispersal varies from dry (self-dispersed) to fleshy (animal-dispersed) fruits. Such variety in reproductive strategies is likely to affect flowering and fruiting phenologies. In this study, we described the reproductive phenology of 81 Melastomataceae species occurring in two biodiversity hotspots: the Atlantic rain forest and the campo rupestre. We aim to disentangle the role of abiotic and biotic factors defining flowering and fruiting times of Melastomataceae species, considering the contrasting breeding and seed dispersal systems, and their evolutionary history. In both vegetation types, pollinator-dependent species had higher flowering seasonality than pollinator-independent ones. Flowering patterns presented phylogenetic signal regardless of vegetation type. Fruiting of fleshy-fruited species was seasonal in campo rupestre but not in Atlantic rain forest; the fruiting of dry-fruited species was also not seasonal in both vegetation types. Fruiting showed a low phylogenetic signal, probably because the influence of environment and dispersal agents on fruiting time is stronger than the phylogenetic affinity. Considering these ecophylogenetic patterns, our results indicate that flowering may be shaped by the different reproductive strategies of Melastomataceae lineages, while fruiting patterns may be governed mainly by the seed dispersal strategy and flowering time, with less phylogenetic influence.
Floral color changes and retention of old flowers are frequently combined phenomena restricted to the floral guide or single flowers in few-flowered inflorescences. They are thought to increase the attractiveness over long distances and to direct nearby pollinators toward the rewarding flowers. In Tibouchina pulchra, a massively flowering tree, the whole flower changes its color during anthesis. On the first day, the flowers are white and on the next 3 days, they change to pink. This creates a new large-scale color pattern in which the white pre-changed flowers contrast against the pink post-changed ones over the entire tree. We describe the spectral characteristics of floral colors of T. pulchra and test bumblebees’ response to this color pattern when viewed at different angles (simulating long and short distances). The results indicated the role of different color components in bumblebee attraction and the possible scenario in which this flower color pattern has evolved. We tested bumblebees’ preference for simulated trees with 75% pink and 25% white flowers resembling the color patterns of T. pulchra, and trees with green leaves and pink flowers (control) in long-distance approach. We also compared an artificial setting with three pink flowers and one white flower (T. pulchra model) against four pink flowers with white floral guides (control) in short-distance approach. Bumblebees spontaneously preferred the simulated T. pulchra patterns in both approaches despite similar reward. Moreover, in short distances, pollinator visits to peripheral, non-rewarding flowers occurred only half as frequently in the simulated T. pulchra when compared to the control. Thefore, this exceptional floral color change and the retention of old flowers in T. pulchra favors the attraction of pollinators over long distances in a deception process while it honestly directs them toward the rewarding flowers at short distances possibly exploring their innate color preferences.
Altitudinal gradients are interesting models to test the effect of biotic and abiotic drivers of floral colour diversity, since an increase in UV irradiance, decrease of pollinator availability and shifts from bee- to fly-pollination in high relative to low altitudes are expected. We tested the effect of altitude and phylogeny, using several chromatic and achromatic colour properties, UV reflectance and pollinators' discrimination capacity (Apis mellifera, Bombus terrestris, Musca domestica and Eristalis tenax), to understand the floral colour diversity in an alpine altitudinal gradient. All colour properties were weakly related to phylogeny. We found a shift from overdispersed floral colours and high chromatic contrast with the background (for bees) in the low altitude, to clustered floral colours (UV and green range for bees and flies) and clustered chromatic and achromatic properties in the high altitude. Different from flies, bees could discriminate floral colours in all altitudinal ranges. Low altitudes are likely to exhibit suitable conditions for more plant species, increasing competition for pollinators and floral colour divergence. Conversely, the increase in UV irradiance in high altitudes may filter plants with specific floral UV-reflectance patterns. Overall, floral colour diversity suggests that both biotic (pollinator fauna) and abiotic (UV irradiance) drivers shape floral communities, but their importance changes with altitude.
Most species in Melastomataceae have poricidal anthers related to specialised bee buzz-pollination, while some have anthers with large openings associated to non-bee pollination systems. We tracked the evolution of anther morphology and seed number on the Miconieae phylogenetic tree to understand the evolutionary shifts in such pollination systems. Anther morphometric data and seed number were recorded for 54 taxa. Pollinators (bees, flies, wasps) were recorded for 20 available species. Ancestral state reconstruction was made using Maximum Likelihood from nrITS sequences. We used phylogenetic eigenvector regressions to estimate phylogenetic signal and the adaptive component for these traits. Species pollinated by bees or bees and wasps tend to have smaller pores and fruits with more seeds. Species pollinated by flies or flies and bees and/or wasps tend to have larger pores and fruits with less seeds. Independent evolution occurred three times for anthers with large pores and twice for fruits with few seeds. We detected a phylogenetic signal in both traits, and negative correlated evolution between them. In actinomorphic small-flowered Miconieae, changes in anther morphology can be related to generalisation in the pollination system incorporating flies and wasps as pollinators and lessening the importance of buzzing bees in such process. Differences in pollen removal and deposition may explain differences in anther morphology and seed number in Miconieae.
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