Flower morphology and plant-bee pollinator interactions are related to stamen dimorphism in Melastomataceae.

Approximately 20,000 species of flowering plant offer mainly pollen to their pollinators, generally bees. Stamen dimorphism, a floral trait commonly present in some pollen flowers, is thought to be associated with exclusive pollen provision for highly effective bee pollinators. Notwithstanding, little is known about how stamen dimorphism is related to other floral morphological traits and, consequently, plant-pollinator interactions at the community scale. Here we investigated the relationship between stamen dimorphism and other floral morphological traits, as well as the interactions with pollinators in plants of Melastomataceae. We characterized each plant species as stamen dimorphic or stamen isomorphic according to differences in size and shape between stamen sets. Data on interactions between the plants and their bee pollinators were analysed as quantitative bipartite networks. We found that petal and style size and shape were correlated to stamen dimorphism. Stamen dimorphic species present larger flowers and less variable style shapes than stamen isomorphic species. Furthermore, stamen dimorphism is associated with higher richness of visiting bees, i.e. higher ecological generalization. During the evolutionary history of Melastomataceae, the dependence on pollinators for fruit set has possibly favoured the evolution of larger flowers with dimorphic stamens, which in turn are able to make use of a larger spectrum of pollen-collecting bees, leading to ecological generalization.

Reproductive phenology of Melastomataceae species with contrasting reproductive systems: contemporary and historical drivers.

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.

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.

Pollination ecology of two species of Elleanthus (Orchidaceae): novel mechanisms and underlying adaptations to hummingbird pollination.

Relationships among floral biology, floral micromorphology and pollinator behaviour in bird-pollinated orchids are important issues to understand the evolution of the huge flower diversity within Orchidaceae. We aimed to investigate floral mechanisms underlying the interaction with pollinators in two hummingbird-pollinated orchids occurring in the Atlantic forest. We assessed floral biology, nectar traits, nectary and column micromorphologies, breeding systems and pollinators. In both species, nectar is secreted by lip calli through spaces between the medial lamellar surfaces of epidermal cells. Such a form of floral nectar secretion has not been previously described. Both species present functional protandry and are self-compatible yet pollinator-dependent. Fruit set in hand-pollination experiments was more than twice that under natural conditions, evidencing pollen limitation. The absence of fruit set in interspecific crosses suggests the existence of post-pollination barriers between these sympatric co-flowering species. In Elleanthus brasiliensis, fruits resulting from cross-pollination and natural conditions were heavier than those resulting from self-pollination, suggesting advantages to cross-pollination. Hummingbirds pollinated both species, which share at least one pollinator species. Species differences in floral morphologies led to distinct pollination mechanisms. In E. brasiliensis, attachment of pollinarium to the hummingbird bill occurs through a lever apparatus formed by an appendage in the column, another novelty to our knowledge of orchid pollination. In E. crinipes, pollinarium attachment occurs by simple contact with the bill during insertion into the flower tube, which fits tightly around it. The novelties described here illustrate the overlooked richness in ecology and morphophysiology in Orchidaceae.

The generalist Inga subnuda subsp. luschnathiana (Fabaceae): negative effect of floral visitors on reproductive success?

Inga species are characterised by generalist or mixed pollination system. However, this feature does not enhance reproductive rates in species with very low fruit set under natural conditions. Some ecological and genetic factors are associated with this feature, and to test the effect of massive visits on pollination success in Inga subnuda subsp. luschnathiana, we studied the efficacy of polyads deposited on stigmas of flowers isolated from visitors and polyads exposed to visitors. The proportion of polyads fixed in stigmas decreased after exposure to visitors (24 h) in comparison to stigmas isolated from visitors (hummingbirds, bees, wasps, hawkmoths and bats), and fruit set was very low. Furthermore, nectar production, sugar composition and other floral biology traits were evaluated. Increased nectar production, sugar availability and sucrose dominance during the night indicates adaptation to nocturnal visitors and supports their role as main pollinators; although the brush-flower morphology, time of anthesis, nectar dynamics and chemical composition also allow daytime visitors. Thus the species is an important resource for a diverse group of floral visitors. We conclude that excess visits (diurnal and nocturnal) are responsible for the decrease in fixed polyads in stigmas of I. subnuda subsp. luschnathiana flowers, thus contributing, with others factors, to its low fruit set. Therefore, the generalist pollination system does not result in reproductive advantages because the low fruit set in natural conditions could be the result of a negative effect of visitors/pollinators.

Beyond the pollination syndrome: nectar ecology and the role of diurnal and nocturnal pollinators in the reproductive success of Inga sessilis (Fabaceae).

Inga species present brush-type flower morphology allowing them to be visited by distinct groups of pollinators. Nectar features in relation to the main pollinators have seldom been studied in this genus. To test the hypothesis of floral adaptation to both diurnal and nocturnal pollinators, we studied the pollination ecology of Inga sessilis, with emphasis on the nectar secretion patterns, effects of sequential removals on nectar production, sugar composition and the role of diurnal and nocturnal pollinators in its reproductive success. Inga sessilis is self-incompatible and pollinated by hummingbirds, hawkmoths and bats. Fruit set under natural conditions is very low despite the fact that most stigmas receive polyads with sufficient pollen to fertilise all ovules in a flower. Nectar secretion starts in the bud stage and flowers continually secreting nectar for a period of 8 h. Flowers actively reabsorbed the nectar a few hours before senescence. Sugar production increased after nectar removal, especially when flowers were drained during the night. Nectar sugar composition changed over flower life span, from sucrose-dominant (just after flower opening, when hummingbirds were the main visitors) to hexose-rich (throughout the night, when bats and hawkmoths were the main visitors). Diurnal pollinators contributed less than nocturnal ones to fruit production, but the former were more constant and reliable visitors through time. Our results indicate I. sessilis has floral adaptations, beyond the morphology, that encompass both diurnal and nocturnal pollinator requirements, suggesting a complementary and mixed pollination system.

Reproductive biology of Cyrtopodium polyphyllum (Orchidaceae): a Cyrtopodiinae pollinated by deceit.

The genus Cyrtopodium comprises about 42 species distributed from southern Florida to northern Argentina. Cyrtopodium polyphyllum occurs on rocks or in sandy soils, in restinga vegetation along the Brazilian coast. It flowers during the wet season and its inflorescences produce a high number of resupinate yellow flowers. Cyrtopodium polyphyllum offers no rewards to its pollinators, but mimics the yellow, reward-producing flowers of nearby growing Stigmaphyllon arenicola (oil) and Crotalaria vitellina (nectar) individuals. Several species of bee visit flowers of C. polyphyllum, but only two species of Centris (Centris tarsata and Centris labrosa) act as pollinators. Visits to flowers of C. polyphyllum were scarce and, as a consequence, low-fruit set was recorded under natural conditions. Such low-fruit production contrasts with the number of fruits each plant bears after manual pollination, suggesting deficient pollen transfer among plants. C. polyphyllum is self-compatible and has a high-fruit set in both manual self- and cross-pollinated flowers. Furthermore, fruits (2%) are formed by self-pollination assisted by rain. This facultative self-pollination mechanism is an important strategy to provide reproductive assurance to C. polyphyllum as rainfall restricts the foraging activity of its pollinating bees. Fruits derived from treatments and under natural conditions had a similar high rate of potentially viable seed. Moreover, these seeds had a low polyembryony rate, which did not exceed 5%. C. polyphyllum acts by deceit involving optical signals and exploits other yellow-flowered species within its habitat by attracting their pollinators. The low capsule production under natural conditions was expected, but its reproductive success is assured through self-pollination by rain and high seed viability.

Phenology and pollination biology of eight Peperomia species (Piperaceae) in semideciduous forests in southeastern Brazil.

Data on flowering phenology and pollination of Peperomia species are virtually non-existent. This study presents data on the pollination biology of eight Peperomia species from south-eastern Brazil, including the flowering phenology, pollination system, and reproductive success. Data on flowering phenology were recorded weekly and exclusion experiments on inflorescences provided data on autonomous self- and wind pollination. Direct visual observations were made and insect visits were recorded. Four Peperomia species showed continuous flowering, while the others were seasonal and flowered in the wet season. Pollination by wind and Syrphidae was confirmed for two self-incompatible Peperomia species. The remaining species are self-compatible and their high fruit set may be accounted for by autonomous self-pollination and perhaps agamospermy. Although the floral morphology of Peperomia species suggests wind- and/or insect pollination, most of the species studied exhibit autogamy and perhaps agamospermy as the main method of reproduction.

The pollination of Bromelia antiacantha (Bromeliaceae) in southeastern Brazil: ornithophilous versus melittophilous features.

Bromelia antiacantha flowered from December to February and during this period the central leaves and bracts displayed a bright red colour. The inflorescence bears 150-350 flowers, with 10-35 flowers opening per day over 4-5 days. The flowers are dark magenta coloured with white margins, tubular-shaped with a wide opening, and their stigma is situated below the anthers. Anthesis began around 4:00 h and flowers lasted approximately 15 h. The highest nectar volume and sugar concentration occurred between 4:00-6:00 h; after this period, both decreased throughout the day. B. antiacantha is partially self-incompatible, non-autogamous, and therefore, pollinator dependent. The hummingbirds Thalurania glaucopis, Amazilia fimbriata, and Ramphodon naevius were its most frequent pollinators (55% of the visits), visiting flowers mainly in the afternoon. The scattered distribution of B. antiacantha promoted trap-lining behaviour of the hummingbirds, which favoured fruit set through xenogamy. Corolla colour, wide flower opening, sweet odour and concentrated nectar early in the day favoured bee visitation. Of the 38 % of bee visits, 96% were made by Bombus morio, mainly in the morning and their behaviour promoted self-pollination. The bee Trigona spinipes frequently acted as a pollen and nectar thief early in the morning, excluding most of the hummingbirds. Bromelia antiacantha has ornithophilous and melittophilous features, and despite being pollinated by two kinds of agents, its reproductive success depends on a given set of circumstances.

Non-Euglossine bees also function as pollinators of Sinningia species (Gesneriaceae) in southeastern brazil.

Pollination by male and female Euglossini bees, euglossophily, was suggested for a number of neotropical Gesneriaceae species. Information on bee species other than Euglossini as pollinators of neotropical members of this family is limited, and in the tribe Sinningieae data about bee pollination are still lacking. Here, we report on floral biology and bee pollination of four Sinningia species: S. schiffneri, S. eumorpha, S. villosa, and Sinningia "canastrensis". The flower features, such as corolla size, shape, and colour, are very different among the four species, but all conform to the melittophilous syndrome. The average nectar volume and sugar amount is low in S. schiffneri, S. eumorpha, and Sinningia "canastrensis", when compared to that of S. villosa, but low nectar amounts is a general feature of Sinningia species. The main pollinators of the four species are: small Tapinotaspidini (Trigonopedia ferruginea) of S. schiffneri, large Bombini (Bombus morio) and large Centridini (Epicharis morio) of S. eumorpha, large Euglossini (Eulaema cingulata and Eufriesea surinamensis) of S. villosa, and large Euglossini (Eufriesea violascens) and Megachilini (Megachile sp.) of Sinningia "canastrensis". Out of the four species, only S. villosa is exclusively Euglossini-pollinated. The marked differences in flower features and nectar production of these Sinningia species may reflect their pollination by distinct groups of bees. These results strengthen the idea of multiple origins for the pollination systems involving bees within this genus, which is highly supported by molecular phylogenetic analyses.