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.

Flower colour within communities shifts from overdispersed to clustered along an alpine altitudinal gradient.

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.

Biomechanical properties of a buzz-pollinated flower.

Approximately half of all bee species use vibrations to remove pollen from plants with diverse floral morphologies. In many buzz-pollinated flowers, these mechanical vibrations generated by bees are transmitted through floral tissues, principally pollen-containing anthers, causing pollen to be ejected from small openings (pores or slits) at the tip of the stamen. Despite the importance of substrate-borne vibrations for both bees and plants, few studies to date have characterized the transmission properties of floral vibrations. In this study, we use contactless laser vibrometry to evaluate the transmission of vibrations in the corolla and anthers of buzz-pollinated flowers of Solanum rostratum, and measure vibrations in three spatial axes. We found that floral vibrations conserve their dominant frequency (300 Hz) as they are transmitted throughout the flower. We also found that vibration amplitude at anthers and petals can be up to greater than 400% higher than input amplitude applied at the receptacle at the base of the flower, and that anthers vibrate with a higher amplitude velocity than petals. Together, these results suggest that vibrations travel differently through floral structures and across different spatial axes. As pollen release is a function of vibration amplitude, we conjecture that bees might benefit from applying vibrations in the axes associated with higher vibration amplification.

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.

The contribution of the BIOTA/FAPESP Program to the knowledge on pollination and plant reproduction / Contribuição do Programa BIOTA/FAPESP para o conhecimento sobre polinização e reprodução em plantas

Abstract Interactions between plant and pollinators are associated with the origin and maintenance of species diversity, as well as ecosystem functioning. The potential of pollination as an ecosystem service is evidenced by its association with food production. Understanding pollination at the landscape scale is essential for characterizing the pollination service for several crops that depend on pollinators for fruit and seed set that make up the human diet. Our aim was to carry out a literature review of studies and projects funded by BIOTA/FAPESP to illustrate the main research approaches developed in the field of Pollination Biology, especially related to plant-pollinator interactions. Plant-pollinator interactions in the Atlantic forest were leveraged as a result of this long-term research program, during which several papers were published in international journals. Pollination by bees (melittophily) was the most representative pollination system studied. In addition to melittophily, other interactions were studied such as pollination by hawkmoths (sphingophily), by hummingbirds (ornithophily) and by bats (chiropterophily). The specific mutualistic relationships between fig trees and fig wasps were also subject of studies within the Program. At the beginning of the BIOTA/FAPESP Program, there were many gaps in basic information about pollination and breeding systems of Brazilian native plant species. Thus, the Program was fundamental to fuel research on the natural history of plants and pollinators from the Atlantic forest. Overall, the Program funded studies that investigated themes such as functional pollination ecology, pollinator effectiveness, plant population genetics, structure and dynamics of plant-pollinator interaction networks, as well as geographic distribution and macroevolution of pollination systems, as well as genetic and molecular studies of native plant populations focusing on pollen flow and genetic structure of populations. Additionally, studies on pollination in the context of landscape ecology had the aim of assessing the effects of forest fragmentation on the functioning of plant populations and their interactions with pollinators and the relationships between landscape structure and ecological processes, biodiversity, and ecosystem service. Therefore, the Program had a prominent role in producing basic data with great implications for understanding the ecology and promoting the conservation of plant-pollinator interactions.

Resumo A interação planta-polinizador está associada à origem e manutenção da diversidade de espécies de plantas e ao funcionamento dos ecossistemas. O potencial da polinização como serviço ecossistêmico é destacado quando associado à produção de alimentos. Compreender esta interação na escala da paisagem é essencial para caracterizar o serviço de polinização para muitos cultivos que dependem dos polinizadores para a formação de frutos e sementes que integram a dieta humana. O objetivo deste trabalho foi realizar uma revisão bibliográfica de estudos e projetos financiados pelo BIOTA/FAPESP para ilustrar as principais abordagens de pesquisa desenvolvidas no campo da Biologia da Polinização, especialmente relacionadas à interação planta-polinizador. As interações planta-polinizador na Mata Atlântica foram alavancadas como resultado desse programa de pesquisa de longo prazo, durante o qual vários artigos foram publicados em revistas internacionais. A polinização por abelhas (melitofilia) foi o sistema de polinização mais representativo estudado. Além da melitofilia, outras interações foram estudadas, como a polinização por mariposas (esfingofilia), por beija-flores (ornitofilia) e por morcegos (quiropterofilia). As relações mutualísticas específicas entre figueiras e vespas do figo também foram objeto de estudos no âmbito do Programa. No início do Programa BIOTA/FAPESP, havia muitas lacunas sobre informações básicas sobre polinização e sistemas de reprodução de espécies vegetais nativas brasileiras. Assim, o Programa foi fundamental para desenvolver pesquisas sobre a história natural de plantas e polinizadores da Mata Atlântica. No geral, o Programa financiou estudos que investigaram temas como ecologia funcional da polinização, eficácia de polinizadores, genética de populações de plantas, estrutura e dinâmica de redes de interação planta-polinizador, bem como distribuição geográfica e macroevolução dos sistemas de polinização, além de estudos genéticos e moleculares de populações de plantas nativas com foco no fluxo de pólen. Adicionalmente, estudos sobre polinização no contexto da ecologia da paisagem tiveram como objetivo avaliar os efeitos da fragmentação florestal no funcionamento das populações de plantas e suas interações com os polinizadores e as relações entre a estrutura da paisagem e os processos ecológicos, biodiversidade e serviços ecossistêmicos. Portanto, o Programa teve um papel de destaque na produção de dados básicos com grandes implicações para o entendimento da ecologia e promoção da conservação das interações planta-polinizador.

Sophora tomentosa e Crotalaria vitellina (Fabaceae): biologia reprodutiva e interações com abelhas na restinga de Ubatuba, São Paulo / Sophora tomentosa and Crotalaria vitellina (Fabaceae): reproductive biology and interactions with bees in the restinga of Ubatuba, São Paulo

O conhecimento das interações entre plantas e seus polinizadores tem-se destacado como ferramenta na biologia da conservação de ambientes degradados, como a Mata Atlântica e no estudo da evolução de características morfológicas que medeiam estas interações. Neste estudo são apresentadas informações sobre a biologia reprodutiva e as interações com os visitantes florais de Sophora tomentosa e Crotalaria vitellina (Fabaceae), espécies comuns em áreas de restinga na Mata Atlântica no Núcleo Picinguaba, Parque Estadual da Serra do Mar, Ubatuba - São Paulo. Estas espécies são sincronopátricas, possuem flores amarelas dispostas em racemos e oferecem néctar como principal recurso. Ambas as espécies são autocompatíveis, mas dependem de polinizadores para formação de frutos e sementes. Xylocopa brasilianorum e Megachile sp.1 foram os polinizadores de S. tomentosa, ao passo que C. vitellina, além destas espécies, também foi polinizada por Bombus morio, Centris labrosa e mais duas espécies de Megachile. Estas espécies de abelhas possuem comprimento da língua compatível com as dimensões das câmaras nectaríferas, acessando o néctar por visitas legítimas. As inflorescências de S. tomentosa foram mais visitadas (0,62 visitas/inflorescência/dia) do que as de C. vitellina (0,37 visitas/inflorescência/dia). Entretanto, em condições naturais, a frutificação em S. tomentosa (33 por cento) é semelhante à de C. vitellina (42 por cento), provavelmente devido às diferenças na eficiência de cada polinizador. Espécies de Trigona e de Augochlora não têm acesso ao néctar em visitas legítimas, pois não possuem comprimento da língua compatível com as dimensões das câmaras nectaríferas. Portanto, as dimensões das câmaras nectaríferas de S. tomentosa e C. vitellina funcionam como barreira seletiva às espécies de abelhas com língua curta, assegurando maior oferta de néctar aos polinizadores. Ainda, os polinizadores destas leguminosas são comuns na restinga e atuam como vetores de pólen de diversas espécies neste ecossistema. Portanto a manutenção destas leguminosas é importante para a diversidade da fauna de abelhas e essencial para a comunidade de plantas.

The study of plant-pollinator interactions is a major tool for conservation biology of fragmented habitats like the Atlantic Rain Forest and for the study of evolutionary traits that rule these interactions. Information on reproductive biology and floral visitor interactions of Sophora tomentosa and Crotalaria vitellina (Fabaceae) is presented in this study. Both species are common in the restinga formation of the Atlantic Rain Forest in the Núcleo Picinguaba, Parque Estadual da Serra do Mar, Ubatuba - São Paulo. These species occur in the same areas, the flowering period is the same for both and they have yellow flowers that offer nectar as the major reward. Both are self-compatible, although fruit and seed set depend on the pollinators. Xylocopa brasilianorum and Megachile sp.1 were pollinators of S. tomentosa, whereas C. vitellina was pollinated by both the aforementioned bees and Bombus morio, Centris labrosa and two separate species of Megachile. All these bees have long tongues and are able to reach nectar at the bottom of the nectar chamber by legitimate visits. The inflorescences of S. tomentosa received more visits (0,62 visits/inflorescence/day) than the inflorescences of C. vitellina (0,37 visits/inflorescence/day). However, the fruit set of S. tomentosa (33 percent) is similar to that of C. vitellina (42 percent) in natural conditions, probably due to different pollinator efficiency. Having shorter tongues, Trigona and Augochlora bees have no access to the nectar chamber by means of legitimate visits. Hence, the dimensions of the nectar chamber of S. tomentosa and C. vitellina act as a selective barrier to short-tongued bees, thus guaranteeing more nectar to the long-tongued visitors. These legume pollinators are very common in the restinga forest, and they act as pollen vectors of other species in this ecosystem as well. The preservation of these legume plants is important to the diversity of bees and essential to the plant community.