Article

Minimum size threshold of visiting bees of a buzz‐pollinated plant species: consequences for pollination efficiency

June 2021
American Journal of Botany 108(6)

DOI:10.1002/ajb2.1681

Authors:

José Mesquita-Neto

Universidad Católica del Maule

Clemens Schlindwein

Federal University of Minas Gerais

Premise: Flowering plants with poricidal anthers are commonly visited by buzzing bees, which vibrate flowers to extract pollen. However, not all flower visitors are in fact pollinators, and features such as body size and duration of flower visits are important factors in determining pollination effectiveness. We tested whether bee-to-flower size relationships predict the pollination effectiveness of flower visitors of a buzz-pollinated species (Chamaecrista ramosa, Fabaceae). Methods: We sorted 13 bee taxa into three groups: smaller than, equivalent to ("fit-size"), and larger than flower herkogamy (spatial separation between anthers and stigma). We expected the latter two groups to touch the stigmas, which would be an indicator of pollination effectiveness, more frequently than the first group. To test this hypothesis, we assessed contact with stigmas, foraging behavior, and duration of visits for the three size groups of bees. Results: Our data reveal that small bees scarcely touched the stigmas, while large and fit-size bees were the most efficient pollinators, achieving high stigma-touching rates, conducting much shorter flower visits, and visiting flowers and conspecific plants at high rates during foraging bouts. Conclusions: The results did not show size-matching among bees and flowers, as expected, but rather a minimum size threshold of efficient pollinators. The finding of such a threshold is a nonarbitrary approach to predicting pollination effectiveness of visitors to herkogamous flowers with poricidal anthers.

Flowers and floral visitors of Chamaecrista ramosa. (A) Flower in front view, showing stigma-anther separation (as), curved petal (*), long curved anthers facing the curved petal (1), short anthers facing the opposite side (2), and gynoecium with stigma at the apex (3). Flower-visiting bees: (B) Xylocopa sp. and (C) Bombus sp. sonicating a flower; (D) Augochlorini and (E) Melipona sp. sonicating groups of anthers; (F) Trigona sp. cutting the anthers to remove pollen; note the flower with anther damage (st = stigma).

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Figures - uploaded by José Mesquita-Neto

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Resource distribution and reproductive efficacy of dimorphic stamens of Senna occidentalis (L.) Link: a case study on the division-of-labour hypothesis

Article

Jul 2024
Rev Bras Botânica

Heteranthery, the presence of different sets of stamens in the same flower, reduces the conflict between effective pollinators and flowers by ensuring adequate resources for the pollinators without affecting reproductive success. Here, we tested the division-of-labour hypothesis in Senna occidentalis, a buzz-pollinated, self-compatible, heterantherous species. The fecundity of pollen grains from long and short stamens was evaluated using hand cross-pollination experiments and by comparing the quantity, size, and quality of pollen in different sets of stamens. The visitation rate and behaviour of floral visitors were also assessed, while their preferences for different sets of stamens were checked using stamen exclusion experiments. The long-pollinating stamens produced a greater number and volume of pollen grains compared to the short-feeding stamens. The pollen grains from long stamens exhibited better germination rates with higher production of fruit and seeds than short stamen pollens in cross-pollination experiments. Nine floral visitors foraged on the flowers, and the large carpenter bees (Xylocopa sp.) were the most dominant and effective pollinators. The long stamens deposited pollen on the lateral and ventral thorax of large-sized pollinators, while the short stamens placed pollen on the ventral and abdomen portions. Therefore, the short stamens might produce pollen grains primarily to feed their pollinators, while the long stamens might generate pollen for pollination and successful fertilization. Further, breeding system experiments indicated a significant pollen limitation and dependency on insect pollination for the increased reproductive outputs (fruit and seed sets). Overall, our findings could indicate a differential distribution of pollen grains in long and short stamens. The differences in the quality and quantity of pollen grains produced by dimorphic stamens of S. occidentalis could fit the division-of-labour hypothesis.

The role of intraspecific variation of bumblebee body size and behavior on buzz pollination of a tropical legume species

Article

Sep 2023
AM J BOT

Premise: Generalized mutualisms have diverse outcomes influenced by partner traits. Although less studied, intraspecific variation of bee traits can be crucial for pollination. We investigated the role of intraspecific body size and behavioral trait variations of bumblebee Bombus morio on the pollination of a buzz-pollinated legume species, Chamaecrista latistipula. Methods: To explore the impact of traits in B. morio (body size and behavior) on C. latistipula pollination, we conducted focused observations of visits to virgin flowers and quantified the removal and deposition of pollen (pollination performance), in addition to fruit and seed formation (reproductive fitness). We measured B. morio body size and their complex behaviors on flowers, including bee vibration descriptors, by analyzing video and sound recordings. Results: We observed intraspecific behavioral differences among B. morio bumblebees associated with different body sizes. Larger bumblebees have half the handling time and vibrational pulses, less angular displacement within flowers, and larger relative peak amplitudes during vibrations than smaller bumblebees. Regardless of their large variation in size and behavior, bumblebees were equally effective in removing pollen and pollinating flowers. The high female reproductive fitness was independent of bumblebee body size and behavior, likely due to the interaction between both. On the other hand, larger bumblebees visited flowers for shorter periods, probably promoting higher male reproductive fitness. Conclusions: This study is the first to highlight the large intraspecific variation of bumblebee body size and behavior in buzz-pollinated flowers in the field. Together, their effects unexpectedly cancel each other, generating a high buzz pollination efficiency. This article is protected by copyright. All rights reserved.

Using geometric morphometrics to determine the "fittest" floral shape: A case study in large-flowered, buzz-pollinated Meriania hernandoi

Article

Jun 2023
AM J BOT

Premise: Floral shape (relative arrangement and position of floral organs) is critical in mediating fit with pollinators and maximizing conspecific pollen transfer particularly in functionally specialized systems. To date, however, few studies have attempted to quantify flowers as the inherently three-dimensional (3D) structures they are and determine the effect of intraspecific shape variation on pollen transfer. We here addressed this research gap using a functionally specialized system, buzz pollination, in which bees extract pollen through vibrations, as a model. Our study species, Meriania hernandoi (Melastomataceae), undergoes a floral shape change from pseudocampanulate corollas with more actinomorphically arranged stamens (first day) to open corollas with a more zygomorphic androecium (second day) over anthesis, providing a natural experiment to test how variation in floral shape affects pollination performance. Methods: In one population of M. hernandoi, we bagged 51 pre-anthetic flowers and exposed half of them to bee pollinators when they were in either stage of their shape transition. We then collected flowers, obtained 3D flower models through x-ray computed tomography for 3D geometric morphometric analyses, and counted the pollen grains remaining per stamen (male pollination performance) and stigmatic pollen loads (female pollination performance). Results: Male pollination performance was significantly higher in open flowers with zygomorphic androecia than in pseudo-campanulate flowers. Female pollination performance did not differ among floral shapes. Conclusions: These results suggest that there is an "optimal" shape for male pollination performance, while the movement of bees around the flower when buzzing the spread-out stamens results in sufficient pollen deposition regardless of floral shape.

Stigmas arrangement, reproductive system, and maternal reproductive success in two species of Stigmaphyllon (Malpighiaceae): does pollinator size matter?

Article

Full-text available

Nov 2021
PLANT ECOL

Most species of Neotropical Malpighiaceae are pollinated by oil-collecting bees of diverse sizes, but the effect of pollinator size on their reproductive success has still not been addressed in the literature. We performed a comparative description of stigma arrangements, analyzing the reproductive system and reproductive success and assessing pollinator sizes in Stigmaphyllon bonariense and Stigmaphyllon jatrophifolium. We collected flowers in three natural populations, conducting pollinator censuses and captures and performing manipulative experiments to determine the plants breeding system. We analyzed the morphology of stigmas and their receptivity and calculated the perimeter of the triangle formed by the stigmas (ST). Pollinator sizes, potential area for pollen transfer (PAPT), and the frequency of visits were also calculated. Stigma arrangement resulted in inverted triangles, and the ST was smaller in S. jatrophifolium than in S. bonariense. The overlap between ST and PAPT suggests that pollinators of all sizes were efficient in pollinating S. jatrophifolium, whereas only large and very large pollinators where efficient in S. bonariense. Moreover, very large pollinators had the highest visit frequencies. Our results indicated that both species are obligate xenog-amous, pollinator-dependent, and present pollen limitation. We observed an increase in reproductive success related to the marked turnover in pollinator assemblage throughout the flowering season. These findings suggest that fruit and seed sets vary according to the context of the pollinators and that large pollinators would have the best performance.

Stigmas arrangement, reproductive system, and maternal reproductive success in two species of Stigmaphyllon (Malpighiaceae): does pollinator size matter?

Article

Full-text available

Sep 2021
PLANT ECOL

Most species of Neotropical Malpighi-aceae are pollinated by oil-collecting bees of diverse sizes, but the effect of pollinator size on their reproductive success has still not been addressed in the literature. We performed a comparative description of stigma arrangements, analyzing the reproductive system and reproductive success and assessing pollinator sizes in Stigmaphyllon bonariense and Stigmaphyllon jatrophifolium. We collected flowers in three natural populations, conducting pollinator censuses and captures and performing manipulative experiments to determine the plants breeding system. We analyzed the morphology of stigmas and their receptivity and calculated the perimeter of the triangle formed by the stigmas (ST). Pollinator sizes, potential area for pollen transfer (PAPT), and the frequency of visits were also calculated. Stigma arrangement resulted in inverted triangles, and the ST was smaller in S. jatrophifolium than in S. bonariense. The overlap between ST and PAPT suggests that pollinators of all sizes were efficient in pollinating S. jatrophifolium, whereas only large and very large pollinators where efficient in S. bonariense. Moreover, very large pollinators had the highest visit frequencies. Our results indicated that both species are obligate xenog-amous, pollinator-dependent, and present pollen limitation. We observed an increase in reproductive success related to the marked turnover in pollinator assemblage throughout the flowering season. These findings suggest that fruit and seed sets vary according to the context of the pollinators and that large pollinators would have the best performance.

Hold tight or loosen up? Functional consequences of a shift in anther architecture depend substantially on bee body size

Article

Full-text available

Aug 2022
OECOLOGIA

A fundamental question in pollination ecology is how pollinators affect the evolution of different floral forms. Yet functional effects of shifts in floral form for plant and pollinator are frequently unclear. For instance, flowers that conceal pollen within tube-like anthers that are spread apart and move freely (free architecture) or are tightly joined together (joined architecture) have evolved independently across diverse plant families and are geographically widespread. Surprisingly, how their bee pollinators affect the function of both architectures remains unknown. We hypothesised that bee body size would affect foraging success and pollination differently for free and joined anther architectures. Therefore, we modified the anther architecture of a single plant species (Solanum elaeagnifolium) and used a single species of generalist bumble bee (Bombus impatiens), which varies greatly in body size. We found that on free anther architecture, larger bees were better pollinators. More pollen on their bodies was available for pollination and they deposited more pollen on stigmas. Conversely, on joined anther architecture, smaller bees were better pollinators. They collected less pollen into their pollen baskets, had more pollen on their bodies available for pollination, and deposited more pollen on stigmas. While we also found modest evidence that plants benefit more from joined versus free anther architecture, further investigation will likely reveal this also depends on pollinator traits. We discuss potential mechanisms by which pollinator size and anther architecture interact and implications for floral evolution.

Transformer Models improve the acoustic recognition of buzz-pollinating bee species

Article

Full-text available

May 2025
ECOL INFORM

Buzz-pollinated crops, such as tomatoes, potatoes, kiwifruit, and blueberries, are among the highest-yielding agricultural products. The flowers of these cultivated plants are characterized by having a specialized flower morphology with poricidal anthers that require vibration to achieve a full seed set. At least 446 bee species, in 82 genera, use floral sonication (buzz pollination) to collect pollen grains as food. Identifying and classifying these diverse often look-alike bee species poses a challenge for taxonomists. Automated classification systems, based upon audible bee floral buzzes, have been investigated to meet this need. Recently, convolutional neural network (CNN) models have demonstrated superior performance in recognizing and distinguishing bee-buzzing sounds compared to classical Machine-Learning (ML) classifiers. Nonetheless, the performance of CNNs remains unsatisfactory and can be improved. Therefore, we applied a novel transformer-based neural network architecture for the task of acoustic recognition of blueberry-pollinating bee species. We further compared the performance of the Audio Spectrogram Transformer (AST) model and its variants, including Self-Supervised AST (SSAST) and Masked Autoencoding AST (MAE-AST), to that of strong baseline CNN models based on previous work, at the task of bee species recognition. We also employed data augmentation techniques and evaluated these models with a data set of bee sounds recorded during visits to blueberry flowers in Chile (518 audio samples of 15 bee species). Our results revealed that Transformer-based Neural Networks combined with pre-training and data augmentation outperformed CNN models (maximum F1-score: 64.5% ± 2; Accuracy: 82.2% ± 0.8). These innovative attention-based neural network architectures have demonstrated exceptional performance in assigning bee buzzing sounds to their respective taxonomic categories, outperforming prior deep learning models. However, transformer approaches face challenges related to small dataset size and class imbalance, similar to CNNs and classical ML algorithms. Combining pre-training with data augmentation is crucial to increase the diversity and robustness of training data sets for the acoustic recognition of bee species. We document the potential of transformer architectures to improve the performance of audible bee species identification, offering promising new avenues for bioacoustic research and pollination ecology.

The invasive bumblebee Bombus terrestris (Linnaeus, 1758) disrupts the adaptive function of heteranthery by indiscriminately visiting the pollinating and feeding anthers of Senna arnottiana flowers

Article

Jun 2024
PLANT BIOLOGY

Heteranthery, the presence of different types of anthers on the same flower, is a floral adaptation that aims to balance the need for pollinators to collect pollen as a food resource while ensuring sufficient pollen for pollination. We investigate the role of heteranthery in the pollination of Senna arnottiana flowers and how it is affected by the behaviour of visiting bee species, with a particular focus on the impact of the invasive bumblebee Bombus terrestris. In three populations of S. arnottiana we measured the size of three sets of anthers and style, stigma–anther separation, pollen quantity and fruit set, and contrasted it with the body size, behaviour, and pollination effectiveness of all floral visitors. Different bee species visited S. arnottiana flowers, and their foraging behaviour varied. Large-bodied native bees, including Centris cineraria, Caupolicana sp. and Cadeguala occidentalis, preferentially visited short anthers, whereas B. terrestris, an exotic bumblebee, foraged from both short and long anthers without distinction. In addition, B. terrestris contacted the stigma at a lower rate than large-bodied native bees. Instead of concentrating its pollen-gathering efforts on the feeding anthers, as predicted by the “division of labor” hypothesis, B. terrestris indiscriminately visited both types of anthers similarly. This behaviour of B. terrestris may disrupt the adaptive significance of heteranthery by mixing the roles of pollination and feeding anthers of S. arnottiana. Therefore, our results highlight the potential disruption of this relationship by exotic pollinators and the need to consider it in conservation efforts.

Intraspecific size shifts in generalist bumblebees and flowers lead to low functional consequences

Article

Full-text available

Sep 2023

Body size is a trait that can affect plant–pollinator interaction efficiency and plant reproductive success. We explored the impact of intraspecific size shifts on the interactions between pollinators and flowering plants under controlled conditions. We considered two development conditions leading to the production of large and small individual flowers of Borago officinalis and Echium plantagineum . We also used the natural variability of worker size within bumblebee colonies to isolate small and large workers. We performed a fully crossed experiment with the two flower sizes of each plant species and the two sizes of bumblebee workers. Our results show that the size of both partners did not affect bee foraging behavior in most of the evaluated parameters and both bee sizes were equally efficient in depositing pollen. Significant differences were found only in pollen deposition across the life of a flower in small flowers of B. officinalis , with the greatest quantity of pollen deposited by small bees. We did not find a relationship between pollinator size and plant fitness. Our results suggest that generalist plant–pollinator interactions may be resilient to future potential mismatches in the size of the partners but remain to be tested if they are still resilient under the new environmental conditions resulting from global changes.

Pollination by native bees achieves high fruit quantity and quality of highbush blueberry: a sustainable alternative to managed pollinators

Article

Full-text available

May 2023

Introduction: Blueberry is one of the most relevant buzz-pollinated crops worldwide, and Chile is the most important global producer of fresh blueberries during wintertime in the Northern Hemisphere. Non-buzzing bees, such as honey bees, may provide suboptimal services compared with bees capable of buzz pollination. The widely held contention that honey bees are inferior pollinators of blueberries drives the industry to place pressure on governments to allow bumblebee (Bombus terrestris) importation for pollination. However, the introduction of B. terrestris generates environmental problems in Chile by competing with and transmitting parasites to local bees. Despite some native Chilean bees being recently recognized as efficient pollen vectors of blueberry crops, no study has evidenced the influence of their visits on fruit yield. Therefore, we aimed to evaluate the native Chilean floral visitors' performance to improve the quantity and quality of highbush blueberry in comparison to the performance of managed visitors.Methods: Per-visit pollination performance (fruit set and fruit quality) and visitation frequency were measured, and the performance of buzzing behavior by flower visitors was evaluated in four cultivars grown in five blueberry orchards located in southern Chile. Results: We found that fruit set and weight were highly influenced by floral visitor taxon. Some native bee species can greatly improve the fruit set and fruit quality (greater weight) of the highbush blueberry cultivars. For instance, one single visit of C. occidentalis can increase fruit weight by a factor of 1.8 compared to an A. mellifera visit; however, visits of halictids and syrphids resulted in lower fruit sets than those of unvisited flowers. However, we found that the occurrence of sonication behavior alone was not a predictor of higher fruit set and fruit weight of highbush blueberry cultivars. Consequently, the taxonomic recognition of floral visitors, ideally to the species level, is still needed to distinguish the most efficient fruit yield promoters of blueberry. Discussion: The conservation of the biotic pollinators, especially native pollinators, would improve blueberry fruit quality and is likely to improve overall crop productivity.

Disparate continental scale patterns in floral host breadth of Australian colletid bees (Colletidae: Hymenoptera)

Article

Full-text available

Mar 2023
APIDOLOGIE

Plant-bee networks are rarely, if ever, studied quantitatively at continental scales, yet these have the potential to inform how biota and ecosystems are assembled beyond narrower regional biomes. The short-tongued bee family Colletidae comprises the major component of bee diversity in Australia, with three key subfamilies: the Neopasiphaeinae, Hylaeinae, and Euryglossinae. We use museum data (> 27,000 records) to record binary interactions between these bees (from each of these subfamilies, resolved to subgenera) and plants (resolved to genera). The resulting networks were analysed using bipartite graphs and associated indices of network structure. The three bee subfamilies showed markedly different network structures with their floral hosts. Euryglossinae had strong interactions with Myrtaceae and an otherwise relatively narrow host breadth, Neopasiphaeinae had little signal of host specialisation above genera and a very broad host breadth, and Hylaeinae appeared intermediate in network structure. Furthermore, Euryglossinae is more speciose within Australia (404 species, or ~ 25% of described Australian bee fauna) than Hylaeinae and Neopasiphaeinae, but these differences do not correspond to the stem ages of the three subfamilies, suggesting that time-since-origin does not explain bee species diversity or floral host breadth. Patterns of host breadth persist after rarefaction analyses that correct for differing numbers of observation records. We suggest that visitation networks could be influenced by evolutionary constraints to expansion of floral host breadth, but it is also possible that many bee-plant interactions are shaped by bees exploiting floral traits that are driven by non-bee fauna operating at large biogeographical scales. Euryglossinae / Hylaeinae / Neopasiphaeinae / Pollination / Myrtaceae

Heteromorphic stamens are differentially attractive in Swartzia (Fabaceae)

Article

Full-text available

Sep 2022

The division of labor hypothesis between stamens has explained the evolution of divergent functions between dimorphic stamens in the same flower. However, little is known about whether the distinct type of stamens differs in attractiveness to pollinators. Therefore, we investigate whether the two types of stamens commonly found in Swartzia have different visual and olfactory attractants. We performed observations of anthesis dynamics, registration and collection of floral visitors, measurements of reflectance of floral parts, and chemical analysis of the volatile organic compounds of the floral parts of two species, S. flaemingii and S. simplex. Both species have two distinct sets of stamens: one with smaller and abundant stamens in the center of the flower and the other with fewer but larger abaxial stamens. The sets differ in UV reflectance (only S. simplex) and exhibit a distinct chromatic contrast. Concerning olfactory attractiveness, aliphatic compounds make up most of the odor of the two species, both whole flowers and most of their floral organs. On the other hand, only S. simplex presented apocarotenoids (as ionones) and benzenoids. Furthermore, there are differences in the proportion of volatiles emitted by the stamen in both cases, as the high proportion of sesquiterpenes among the smaller stamens compared to the larger ones. In conclusion, the two types of stamens found in S. flaemingii and S. simplex show a distinct attractiveness. In addition, our data have demonstrated diverse ways of differential attractiveness both between distinct stamens set per flower and between the two species from the same pollen flowers genus

Native bees with floral sonication behaviour can achieve high‐performance pollination of highbush blueberry in Chile

Article

Full-text available

Aug 2022

Blueberry is one of the most relevant buzz‐pollinated crops worldwide and Chile is the most important global producer of fresh blueberries during wintertime in the Northern Hemisphere. Thousands of exotic Bombus terrestris are imported from Europe to pollinate blueberries. However, no study has investigated the performance of the native Chilean fauna to pollinate blueberry or other crops. Therefore, we aimed to compare the performance of native Chilean floral visitors with managed visitors to pollinate highbush blueberry. Per‐visit pollination performance (stigmatic pollen deposition) and floral visitation were measured and the presence of sonication behaviour of flower visitors was evaluated for five cultivars in two blueberry orchards located in southern Chile. Floral visitors showed a preference for one or more blueberry cultivars, instead of visiting all cultivars equally. Floral visits with sonication deposited more conspecific pollen on stigmas than visits without sonication. Some native sonicating bees ( Cadeguala and Bombus ), especially Cadeguala occidentalis , were efficient pollen vectors of blueberry and better pollinators than honeybees (5.8 times more pollen transferred) similar to that of the managed bee B. terrestris . The results indicate that some Chilean native bee species, especially those with sonication behaviour, can provide pollination service to highbush blueberry crops.

Anther cones increase pollen release in buzz‐pollinated Solanum flowers

Article

Full-text available

Mar 2022

The widespread evolution of tube‐like anthers releasing pollen from apical pores is associated with buzz pollination, in which bees vibrate flowers to remove pollen. The mechanical connection among anthers in buzz‐pollinated species varies from loosely held conformations, to anthers tightly held together with trichomes or bio‐adhesives forming a functionally joined conical structure (anther cone). Joined anther cones in buzz‐pollinated species have evolved independently across plant families and via different genetic mechanisms, yet their functional significance remains mostly untested. We used experimental manipulations to compare vibrational and functional (pollen release) consequences of joined anther cones in three buzz‐pollinated species of Solanum (Solanaceae). We applied bee‐like vibrations to focal anthers in flowers with (“joined”) and without (“free”) experimentally created joined anther cones, and characterised vibrations transmitted to other anthers and the amount of pollen released. We found that joined anther architectures cause non‐focal anthers to vibrate at higher amplitudes than free architectures. Moreover, in the two species with naturally loosely held anthers, anther fusion increases pollen release, while in the species with a free but naturally compact architecture it does not. We discuss hypotheses for the adaptive significance of the convergent evolution of joined anther cones. This article is protected by copyright. All rights reserved

Machine learning approach for automatic recognition of tomato-pollinating bees based on their buzzing-sounds

Article

Full-text available

Sep 2021
PLOS COMPUT BIOL

Bee-mediated pollination greatly increases the size and weight of tomato fruits. Therefore, distinguishing between the local set of bees–those that are efficient pollinators–is essential to improve the economic returns for farmers. To achieve this, it is important to know the identity of the visiting bees. Nevertheless, the traditional taxonomic identification of bees is not an easy task, requiring the participation of experts and the use of specialized equipment. Due to these limitations, the development and implementation of new technologies for the automatic recognition of bees become relevant. Hence, we aim to verify the capacity of Machine Learning (ML) algorithms in recognizing the taxonomic identity of visiting bees to tomato flowers based on the characteristics of their buzzing sounds. We compared the performance of the ML algorithms combined with the Mel Frequency Cepstral Coefficients (MFCC) and with classifications based solely on the fundamental frequency, leading to a direct comparison between the two approaches. In fact, some classifiers powered by the MFCC–especially the SVM–achieved better performance compared to the randomized and sound frequency-based trials. Moreover, the buzzing sounds produced during sonication were more relevant for the taxonomic recognition of bee species than analysis based on flight sounds alone. On the other hand, the ML classifiers performed better in recognizing bees genera based on flight sounds. Despite that, the maximum accuracy obtained here (73.39% by SVM) is still low compared to ML standards. Further studies analyzing larger recording samples, and applying unsupervised learning systems may yield better classification performance. Therefore, ML techniques could be used to automate the taxonomic recognition of flower-visiting bees of the cultivated tomato and other buzz-pollinated crops. This would be an interesting option for farmers and other professionals who have no experience in bee taxonomy but are interested in improving crop yields by increasing pollination.

Using Historic Data to Understand the Shrinking Pollinators of the Endangered Salt Marsh Bird's Beak (Chloropyron maritimum subsp. Maritimum)

Article

Jan 2024

Harvesting pollen with vibrations: Towards an integrative understanding of the proximate and ultimate reasons for buzz pollination

Article

Full-text available

Dec 2023
ANN BOT-LONDON

Buzz pollination, a type of interaction in which bees use vibrations to extract pollen from certain kinds of flowers, captures a close relationship between thousands of bee and plant species. In the last 120 years, studies of buzz pollination have contributed to our understanding of the natural history of buzz pollination, and basic properties of the vibrations produced by bees and applied to flowers in model systems. Yet, much remains to be done to establish its adaptive significance and the ecological and evolutionary dynamics of buzz pollination across diverse plant and bee systems. Here, we review for bees and plants the proximate (mechanism and ontogeny) and ultimate (adaptive significance and evolution) explanations for buzz pollination, focusing especially on integrating across these levels to synthesise and identify prominent gaps in our knowledge. Throughout, we highlight new technical and modelling approaches and the importance of considering morphology, biomechanics, and behaviour in shaping our understanding of the adaptive significance of buzz pollination. We end by discussing the ecological context of buzz pollination and how a multilevel perspective can contribute to explain the proximate and evolutionary reasons for this ancient bee-plant interaction.

Hold tight or loosen up? Functional consequences of a shift in anther architecture depend substantially on bee body size

Preprint

Full-text available

May 2022

A fundamental question in pollination ecology is how pollinators affect the evolution of different floral forms. Yet functional effects of shifts in floral form for plant and pollinator are frequently unclear. For instance, flowers that conceal pollen within tube-like anthers that are spread apart and move freely (free architecture) or are tightly joined together (joined architecture) have evolved independently across diverse plant families and are geographically widespread. Surprisingly, how their bee pollinators affect the function of both architectures remains unknown. We hypothesized that bee body size would affect foraging success and pollination differently for free and joined anther architectures. We therefore modified the anther architecture of a single plant species ( Solanum elaeagnifolium ) and used a single species of generalist bumble bee ( Bombus impatiens ), which varies greatly in body size. We found that on free anther architecture, larger bees were better pollinators. More pollen on their bodies was available for pollination and they deposited more pollen on stigmas. Conversely, on joined anther architecture, smaller bees were better pollinators. They collected less pollen into their pollen baskets, had more pollen on their bodies available for pollination, and deposited more pollen on stigmas. While we also found modest evidence that plants benefit more from joined versus free anther architecture, further investigation will likely reveal this also depends on pollinator traits. We discuss potential mechanisms by which pollinator size and anther architecture interact and implications for floral evolution.

Anther cones increase pollen release in buzz-pollinated Solanum flowers

Preprint

Full-text available

Oct 2021

The widespread evolution of tube-like anthers releasing pollen from apical pores is associated with buzz pollination, in which bees vibrate flowers to remove pollen. The mechanical connection among anthers in buzz-pollinated species varies from loosely held conformations, to anthers tightly held together with trichomes or bio-adhesives forming a functionally joined conical structure (anther cone). Joined anther cones in buzz-pollinated species have evolved independently across plant families and via different genetic mechanisms, yet their functional significance remains mostly untested. We used experimental manipulations to compare vibrational and functional (pollen release) consequences of joined anther cones in three buzz-pollinated species of Solanum (Solanaceae). We applied bee-like vibrations to focal anthers in flowers with ('joined') and without ('free') experimentally created joined anther cones, and characterised vibrations transmitted to other anthers and the amount of pollen released. We found that joined anther architectures cause non-focal anthers to vibrate at higher amplitudes than free architectures. Moreover, in the two species with naturally loosely held anthers, anther fusion increases pollen release, while in the species with a free but naturally compact architecture it does not. We discuss hypotheses for the adaptive significance of the convergent evolution of joined anther cones.

THE CONSEQUENCES OF FLORAL HERBIVORY FOR POLLINATOR SERVICE TO ISOMERIS ARBOREA

Article

Full-text available

Jan 1999

Beyond robbery: the role of upside-down behaviour performed by small oil-collecting bees in Malpighiaceae

Article

Full-text available

Oct 2020
ARTHROPOD-PLANT INTE

In plant–pollination interactions, the antagonists collect the same set of resources offered to legitimate visitors, but their morphologies and behavioural approaches possibly make their effect on plant fitness negative rather than positive. Depending on the morphology of Malpighiaceae flowers, these small-bodied bees can adopt an upside-down position, biting and damaging the floral pedicel. Therefore, we hypothesized that small-bodied bees may reduce female reproductive fitness, due to increased floral abscission. We observed small Tetrapedia bees approaching bagged and unbagged flowers of Peixotoa tomentosa, and compared abscission rates associated with the upside-down behavior performance. When Tetrapedia bees exhibited the upside-down behaviour the floral abscission was about 1.7 times more frequent than without this behaviour. We observed that abscission frequency increased to 80% if upside-down behavior is performed at least three times per flower. Additionally, the frequency of upside-down behaviours were positively related to the number of flowers visited per plant. Overall, the upside-down behaviour of Tetrapedia compromised most flowers that were viable for fruit formation, potentially decreasing the female reproductive fitness of plant population. We emphasize that different roles of floral visitors, including the robbers, are associated with visitors’ body size and behaviour. Such features of interactions determine whether floral visitors are pollinators, thieves or robbers and shape a continuum from mutualistic to antagonistic interactions.

Morphological specialisation of heterantherous Rhynchanthera grandiflora (Melastomataceae) accommodates pollinator diversity

Article

Full-text available

Feb 2020

The tropical Melastomataceae are characterized by poricidal anthers which constitute a floral filter selecting for buzz‐pollinating bees. Stamens are often dimorphic, sometimes with discernible feeding and pollinating functions. Rhynchanthera grandiflora produces nectarless flowers with four short stamens and one long stamen; all anthers feature a narrow elongation with an upwards facing pore. We tested pollen transfer by diverse foraging bees and viability of pollen from both stamen types. The impact of anther morphology on pollen release direction and scattering angle was studied to determine the plant's reproductive strategy. Medium‐sized to large bees sonicated flowers in a specific position, and the probability of pollen transfer correlated with bee size even among these legitimate visitors. Small bees acted as pollen thieves or robbers. Anther rostrum and pore morphology serve to direct and focus the pollen jet released by floral sonication towards the pollinator's body. Resulting from the ventral and dorsal positioning of the short and long stamens, respectively, the pollinator's body was widely covered with pollen. This improves the plant's chances of outcrossing, irrespective of which bee body part contacts the stigma. Consequently, R. grandiflora is also able to employ bee species of various sizes as pollen vectors. The strategy of spreading pollen all over the pollinator's body is rather cost‐intensive but counterbalanced by ensuring that most of the released pollen is in fact transferred to the bee. Thus, flowers of R. grandiflora illustrate how specialized morphology may serve to improve pollination by a functional group of pollinators.

Patterns of pollen flow in monomorphic enantiostylous species: the importance of floral morphology and pollinators’ size

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Feb 2020

Enantiostyly is a floral polymorphism consisting in the presence of two floral morphs that differ in the deflection of the style to the right or left in the populations. Monomorphic enantiostyly consists in plants showing both morphs within an individual and is thought to promote pollen transference between morphs, reduce levels of self-pollination and geitonogamy and avoid damage to floral parts during pollinator’s visit. In this study, we examined the function of this floral polymorphism in a group of plants with non-typical enantiostylous characteristics, the family Vochysiaceae. In particular, we evaluated how floral morphology (both sexual organ separation and the match between complementary sexual organs in the morphs) is related to pollen deposition on the pollinators’ body and to patterns of pollen flow among individuals. For this, we used floral morphometrics, insect captures and fluorescent powder dyes. We confirmed that monomorphic enantiostyly increased pollen transference between morphs compared to non-enantiostyly. Moreover, pollen flow occurred only between flowers of opposite morph. We also observed that pollen deposition on the insect’s body depended on their body shape rather than floral morphology. In fact, an intertegular distance slightly larger than the anther–stigma distance in the flowers increased pollen transference because anthers filaments and stigmas are flexible, which facilitated pollen brushing on insects’ body when approaching the flowers. Since the species are self-incompatible, we further discuss the role of mirror flowers in the reduction of geitonogamy and inbreeding depression.

O gênero Chamaecrista (Leguminosae: Caesalpinioideae) no Parque Estadual do Rio Preto, São Gonçalo do Rio Preto, Minas Gerais, Brasil

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Jan 2019

Resumo O gênero Chamaecrista possui distribuição pantropical e está bem representado na flora brasileira, principalmente em campos rupestres e matas ciliares. No Brasil são encontradas 256 espécies, sendo que 149 delas aparecem somente em Minas Gerais, o que corresponde mais da metade da diversidade do gênero no país. A área selecionada para o estudo, o Parque Estadual do Rio Preto (PERP), pertence à Cadeia do Espinhaço. A vegetação é composta principalmente por fitofisionomias de Cerrado e Campo rupestre existindo também áreas de matas ciliares e de galerias. O estudo em questão teve como objetivo realizar o levantamento florístico e um estudo taxonômico de Chamaecrista no PERP, abrangendo chave de identificação das espécies e descrições taxonômicas das mesmas. As coletas foram realizadas dentro de um período de dois anos, por meio de caminhadas assistemáticas. O material coletado foi identificado e depositado na coleção do Herbário OUPR. Foram coletados e descritos 19 táxons que compreendem às seções Absus, Chamaecrista e Xerocalyx.

Big bees do a better job: intraspecific size variation influences pollination effectiveness

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Sep 2014

• Bumblebees (Bombus spp.) are efficient pollinators of many flowering plants, yet the pollen deposition performance of individual bees has not been investigated. Worker bumblebees exhibit large intraspecific and intra-nest size variation, in contrast with other eusocial bees; and their size influences collection and deposition of pollen grains. • Laboratory studies with B. terrestris workers and Vinca minor flowers showed that pollen grains deposited on stigmas in single visits (SVD) were significantly positively related to bee size; larger bees deposited more grains, while the smallest individuals, with proportionally shorter tongues, were unable to collect or deposit pollen in these flowers. Individuals did not increase their pollen deposition over time, so handling experience does not influence SVD in Vinca minor. • Field studies using Geranium sanguineum and Echium vulgare, and multiple visiting species, confirmed that individual size affects SVD. All bumblebee species showed size effects, though even the smallest individuals did deposit pollen, whereas there was no detectable effect with Apis with its limited size variation. Two abundant hoverfly species also showed size effects, particularly when feeding for nectar. • Mean size of foragers also varied diurnally, with larger individuals active earlier and later, so that pollination effectiveness varies through a day; flowers routinely pollinated by bees may best be served by early morning dehiscence and visits from larger individuals. • Thus, while there are well-documented species-level variations in pollination effectiveness, the fine-scale individual differences between foragers should also be taken into account when assessing the reproductive outputs of biotically-pollinated plants.

More on Buzz Pollination—Pollen Rebounds in Asymmetric Flowers

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Mar 2019

Does body size predict the buzz-pollination frequencies used by bees?

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Mar 2019

Body size is an important trait linking pollinators and plants. Morphological matching between pollinators and plants is thought to reinforce pollinator fidelity, as the correct fit ensures that both parties benefit from the interaction. We investigated the influence of body size in a specialized pollination system (buzz‐pollination) where bees vibrate flowers to release pollen concealed within poricidal stamens. Specifically, we explored how body size influences the frequency of buzz‐pollination vibrations. Body size is expected to affect frequency as a result of the physical constraints it places on the indirect flight muscles that control the production of floral vibrations. Larger insects beat their wings less rapidly than smaller‐bodied insects when flying, but whether similar scaling relationships exist with floral vibrations has not been widely explored. This is important because the amount of pollen ejected is determined by the frequency of the vibration and the displacement of a bee's thorax. We conducted a field study in three ecogeographic regions (alpine, desert, grassland) and recorded flight and floral vibrations from freely foraging bees from 27 species across four families. We found that floral vibration frequencies were significantly higher than flight frequencies, but never exceeded 400 Hz. Also, only flight frequencies were negatively correlated with body size. As a bee's size increased, its buzz ratio (floral frequency/flight frequency) increased such that only the largest bees were capable of generating floral vibration frequencies that exceeded double that of their flight vibrations. These results indicate size affects the capacity of bees to raise floral vibration frequencies substantially above flight frequencies. This may put smaller bees at a competitive disadvantage because even at the maximum floral vibration frequency of 400 Hz, their inability to achieve comparable thoracic displacements as larger bees would result in generating vibrations with lower amplitudes, and thus less total pollen ejected for the same foraging effort.

The effect of a flower-dwelling predator on a specialized pollination system

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Mar 2019

Plant species vary greatly in the number and diversity of floral visitors with which they interact. Even so, pollination ecologists have focused mainly on direct pairwise interactions (mutualists), overlooking indirect effects produced by different agents, such as floral larcenists and flower-dwelling predators. In our study area in Brazil, the pollen flowers of Chamaecrista ramosa (Fabaceae) harbour Misumenops sp. (Thomisidae) spiders, a flower-dwelling predator with unknown signalling strategy. We measured the effect of Misumenops on the foraging behaviour of three bee species, one behaving as a pollen robber (Trigona spinipes) and two as pollinators (Xylocopa ordinaria and X. hirsutissima), and the consequences for plant fitness. The presence of Misumenops reduced the frequency of Trigona bee visits and increased the proportion of undamaged anthers, and thus pollen available to Xylocopa bees, which seemed unaffected by spider presence. However, spider presence (detectable by both Trigona and Xylocopa bees through achromatic and chromatic contrasts) had no effect on fruit and seed set when compared to flowers without spiders. Thus, the apparently antagonistic interaction between Trigona and flowers can represent a commensalism, modulated by differences between pollinators and larcenists regarding the window of foraging activity, as well as regarding foraging efficiency. The results also indicate that the quantitative impact of predators of floral visitor on plant fitness will be highly dependent on context in species with specialized pollination systems.

Trade off between quantity and size of pollen grains in the heterandrous flowers of Senna pendula (Fabaceae)

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Jul 2018

Heteranthery, the presence of different types of stamens in a flower, may reduce the conflict between pollinators and plants by ensuring the resource for the pollinator without drastically affecting the availability of viable male gametes for fertilization, according to the division-of-labor hypothesis. We investigated whether the poricidal anthers of Senna pendula, a buzz-pollinated heterantherous species, present morphological and physiological differences among pollen grains from the three sets of stamens. We compared quantity, ornamentation, size and fecundity of pollen from long, medium and short stamens. The short feeding stamens produced larger but fewer pollen grains than the long pollinating stamens, which produced smaller pollen grains but in higher quantity. The total pollen volume of pollinating and feeding stamens per flower, however, was the same. The medium stamen produced less-fertile small pollen grains and seems to play no specific role in bee feeding and pollination. Our results indicate differential allocation of pollen for pollinating and feeding stamens mediated by heteranthery. The differences in volume versus quantity of pollen grains fit the division-of-labor hypothesis well for heterantherous pollen-only flowers with poricidal anthers.

The evolution of floral sonication, a pollen foraging behavior used by bees (Anthophila)

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Jan 2018
EVOLUTION

Over 22,000 species of biotically pollinated flowering plants, including some major agricultural crops, depend primarily on bees capable of floral sonication for pollination services. The ability to sonicate (“buzz”) flowers is widespread in bees but not ubiquitous. Despite the prevalence of this pollinator behavior and its importance to natural and agricultural systems, the evolutionary history of floral sonication in bees has not been previously studied. Here, we reconstruct the evolutionary history of floral sonication in bees by generating a time-calibrated phylogeny and reconstructing ancestral states for this pollen extraction behavior. We also test the hypothesis that the ability to sonicate flowers and thereby efficiently access pollen from a diverse assemblage of plant species, led to increased diversification amongst sonicating bee taxa. We find that floral sonication evolved on average 45 times within bees, possibly first during the Early Cretaceous (100-145 million years ago) in the common ancestor of bees. We find that sonicating lineages are significantly more species rich than non-sonicating sister lineages when comparing sister clades, but a probabilistic structured rate permutation on phylogenies approach failed to support the hypothesis that floral sonication is a key driver of bee diversification. This study provides the evolutionary framework needed to further study how floral sonication by bees may have facilitated the spread and common evolution of angiosperm species with poricidal floral morphology.

Does the morphological fit between flowers and pollinators affect pollen deposition? An experimental test in a buzz-pollinated species with anther dimorphism

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Mar 2017

Some pollination systems, such as buzz-pollination, are associated with floral morphologies that require a close physical interaction between floral sexual organs and insect visitors. In these systems, a pollinator's size relative to the flower may be an important feature determining whether the visitor touches both male and female sexual organs and thus transfers pollen between plants efficiently. To date, few studies have addressed whether in fact the “fit” between flower and pollinator influences pollen transfer, particularly among buzz-pollinated species. Here we use Solanum rostratum, a buzz-pollinated plant with dimorphic anthers and mirror-image flowers, to investigate whether the morphological fit between the pollinator's body and floral morphology influences pollen deposition. We hypothesized that when the size of the pollinator matches the separation between the sexual organs in a flower, more pollen should be transferred to the stigma than when the visitor is either too small or too big relative to the flower. To test this hypothesis, we exposed flowers of S. rostratum with varying levels of separation between sexual organs, to bumblebees (Bombus terrestris) of different sizes. We recorded the number of visits received, pollen deposition, and fruit and seed production. We found higher pollen deposition when bees were the same size or bigger than the separation between anther and stigma within a flower. We found a similar, but not statistically significant pattern for fruit set. In contrast, seed set was more likely to occur when the size of the flower exceeded the size of the bee, suggesting that other postpollination processes may be important in translating pollen receipt to seed set. Our results suggest that the fit between flower and pollinator significantly influences pollen deposition in this buzz-pollinated species. We speculate that in buzz-pollinated species where floral morphology and pollinators interact closely, variation in the visitor's size may determine whether it acts mainly as a pollinator or as a pollen thief (i.e., removing pollen rewards but contributing little to pollen deposition and fertilization).

Polliantion ecology of Desmodium setigerum (Fabaceae) in Uganda; do big bees do it better?

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Aug 2016

Explosive pollen release is documented in many plant families, including the Fabaceae. Desmodium setigerum E. Mey (Fabaceae) is a perennial herb with single trip explosive pollen release found in eastern Africa, and the unique ability to reverse floral colour change if insufficient pollination has occurred. However, little else is known about the pollination ecology of this species, what visitors can trigger explosive pollen release, and whether bee body size is related to pollination efficiency. We investigated: 1) the breeding system of D. setigerum, and whether it is pollen limited; 2) whether flowers are visited early in the day allowing sufficient time for a second opportunity for pollination; and 3) what insect species visit D. setigerum and the relative efficacy of different flower visitors in relation to visitor size and pollination success. We found that although self-compatible, D. setigerum requires insect visitation to set seed as explosive pollen release is needed even for selfing. Most flowers are initially visited before 1400h, and by 1800h nearly all flowers have been tripped. Flowers were not pollen limited in this study, and were visited primarily by bees. We observed 16 visiting species, and there was a wide variation (0-404 grains) in the amount of pollen deposited on stigmas. Although almost all bees deposited some pollen, the mean number of pollen grains deposited in a single visit per species was negatively related to body size. However, one particular megachilid species deposited significantly more pollen grains than any other visitor and so is likely an important pollinator of this species. This provides insights into the pollination biology of this unique plant species, and adds to increasing literature on the relationships between bee body size, explosive pollen release and pollination effectiveness.

Bees collecting pollen from flowers with poricidal anthers in a south Brazilian Araucaria forest: A community study

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Jan 2002

A community study of bees visiting flowers with poricidal anthers was made in the subtropical Araucaria forest region of Rio Grande do Sul, Brazil. Bees of 79 species, representing about 40% of the taxa occurring at the study site, were collected on 19 species of flowering plants with poricidal anthers of the families Melastomataceae and Solanaceae. The majority of flower visitors were able to buzz (sonicate) to release pollen. Buzzing is thought to be the only mode of pollen collection that results in pollination. No oligolectic bee-plant relation based on buzz pollination was detected. Most bees were not specialized to forage on plants with poricidal anthers. According to the abundance of visitors at specific flowers, three major groups of buzz pollinators could be distinguished; these were bumble bees, stingless bees of the genus Melipona and halictid bees. The pollen sources mainly exploited by them differ in flower structure, flowering syndrome and forest stratum. Therefore, the structure of the bee community seems to be closely related to the composition of the local vegetation. The extent to which bees of a species show preference for poricidal flowers, however, is more dependent on habitat than on plant taxa. The evolution of buzzing behaviour by female bees to maximize pollen harvest may have preceded the appearance of poricidal anthers and the syndrome of buzz pollination.

Pollination Ecology: A Practical Approach

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Jan 1992

Amots Dafni

Evolution of flower structures and pollination in Neotropical Cassiinae (Caesalpiniaceae) species

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Jan 1988

High incidence of pollen theft in natural populations of a buzz-pollinated plant

Article

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Dec 2015
ARTHROPOD-PLANT INTE

More than 20,000 angiosperm species possess non-dehiscent anthers that open through small pores at the anther’s tip. These flowers are visited by bees that use vibrations to remove pollen, a phenomenon known as buzz pollination. However, some floral visitors fail to transfer pollen efficiently, either through a mismatch of flower and insect size, or because they are unable to buzz-pollinate. These visitors collect pollen, but provide little or no pollination, behaving as pollen thieves. Although pollen theft is widespread in plants, few studies have quantified the incidence of pollen thieves for buzz-pollinated plants. We use observations of natural populations and floral manipulations of Solanum rostratum (Solanaceae) to investigate the incidence of pollen theft, find morphological and behavioural differences between pollinators and thieves, measure the pollination efficiency of visitors, and characterize the reproductive ecology of this herb. We found that most visitors act as thieves, with <20 % of all bees contacting the stigma. Insect visitors that regularly failed to contact the stigma (illegitimate visitors), included buzzing and non-buzzing bees, were significantly smaller, visited fewer flowers per bout, and stayed longer in each flower than (legitimate) visitors that regularly contact the stigma. Few flowers visited solely by illegitimate visitors set fruit. Our results show that S. rostratum requires insect visitation to set seed and natural populations experience moderate pollen limitation. We conclude that insect size, relative to the flower, is the main determinant of whether a visitor acts as a pollinator or a pollen thief in S. rostratum.

Breeding systems of enantiostylous Cassiinae species (Fabaceae, Caesalpinioideae)

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Aug 2015
FLORA

In the right place at the right time: Parnassia resolves the herkogamy dilemma by accurate repositioning of stamens and stigmas

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Nov 2013
ANN BOT-LONDON

Background and AimsSpatial (herkogamy) and temporal (dichogamy) separation of pollen presentation and stigma receptivity have been interpreted as reducing interference between male and female functions in hermaphroditic flowers. However, spatial separation leads to a potential conflict: reduced pollination accuracy, where pollen may be placed in a location on the pollinator different from the point of stigma contact.Methods To understand better how herkogamous flowers resolve this conflict, a study was made of a subalpine herb, Parnassia epunctulata, the nectariferous flowers of which exhibit sequential anther dehiscence (staggered pollen presentation) and stamen movements; usually one newly dehisced anther is positioned each day over the central gynoecium, while the older stamens bend away from the central position.Key ResultsThe open flowers were visited by a variety of pollinators, most of which were flies. Seed set was pollinator-dependent (bagged flowers set almost no seeds) and pollen-limited (manual pollination increased seed set over open pollination). Analyses of adaptive accuracy showed that coordinated stamen movements and style elongation (movement herkogamy) dramatically increased pollination accuracy. Specifically, dehiscing anthers and receptive stigmas were positioned accurately in the vertical and horizontal planes in relation to the opposite sexual structure and pollinator position. By contrast, the spatial correspondence between anthers and stigma was dramatically lower before the anthers dehisced and after stamens bent outwards, as well as before and after the period of stigmatic receptivity.Conclusions It is shown for the first time that a combination of movement herkogamy and dichogamy can maintain high pollination accuracy in flowers with generalized pollination. Staggered pollen and stigma presentation with spatial correspondence can both reduce sexual interference and improve pollination accuracy.

The Consequences of Floral Herbivory for Pollinator Service to Isomeris arborea

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Jan 1999

Flower-feeding insects may reduce the reproductive success of their host plant in subtle ways that go beyond a direct reduction in gametes. Pollinators may respond to floral damage by visiting damaged plants at lower rates. Fewer visitations to the plant may result in fewer flowers that receive pollinator service and as a consequence lead to lower male and/or female reproductive success. In a two-year study, we examined the direct effect of flower predation by Meligethes rufimanus on the floral display of Isomeris arboreal and the indirect effect of herbivory on pollinator behavior. Plants exposed to herbivore attack produced fewer functional inflorescences than plants protected from herbivory. Un- damaged flowers produced three times as much nectar per flower as damaged flowers. Likewise, protected plants had over twice as many anthers per flower as exposed plants. Pollinators responded by visiting damaged flowers less, and exposed plants had lower flower visitation rates than protected plants. Pollinators also visited patches of protected plants more frequently than exposed patches. These results show that floral herbivory reduces pollinator service and thus may reduce reproductive success indirectly, as well as through the direct consumption of viable gametes.

Variability in bumblebee pollination buzzes affects the quantity of pollen released from flowers

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Nov 2012
OECOLOGIA

Buzz-pollination is a plant strategy that promotes gamete transfer by requiring a pollinator, typically bees (Hymenoptera: Apoidea), to vibrate a flower's anthers in order to extract pollen. Although buzz-pollination is widespread in angiosperms with over 20,000 species using it, little is known about the functional connection between natural variation in buzzing vibrations and the amount of pollen that can be extracted from anthers. We characterized variability in the vibrations produced by Bombus terrestris bumblebees while collecting pollen from Solanum rostratum (Solanaceae), a buzz-pollinated plant. We found substantial variation in several buzzing properties both within and among workers from a single colony. As expected, some of this variation was predicted by the physical attributes of individual bumblebees: heavier workers produced buzzes of greater amplitude. We then constructed artificial "pollination buzzes" that varied in three parameters (peak frequency, peak amplitude, and duration), and stimulated S. rostratum flowers with these synthetic buzzes to quantify the relationship between buzz properties and pollen removal. We found that greater amplitude and longer duration buzzes ejected substantially more pollen, while frequency had no directional effect and only a weak quadratic effect on the amount of pollen removed. These findings suggest that foraging bumblebees may improve pollen collection by increasing the duration or amplitude of their buzzes. Moreover, given that amplitude is positively correlated with mass, preferential foraging by heavier workers is likely to result in the largest pollen yields per bee, and this could have significant consequences for the success of a colony foraging on buzz-pollinated flowers.

Enantiostyly in Chamaecrista ramosa (Fabaceae-Caesalpinioideae): Floral morphology, pollen transfer dynamics and breeding system

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Nov 2012
PLANT BIOLOGY

Enantiostyly is a form of reciprocal herkogamy, in which floral morphs present reciprocal differences in the position of sexual elements, and occurs in monomorphic and dimorphic forms. This polymorphism maximises cross-pollination and reduces self-pollination, being very common within the subtribe Cassiinae (Fabaceae). Nevertheless, few studies have investigated the functionality of enantiostyly, particularly in this plant group. The present study aimed to investigate enantiostyly and its functionality in Chamaecrista ramosa, a monomorphic enantiostylous shrub, in an area of coastal vegetation in northeast Brazil. Pollen deposition and capture on the body of floral visitors, the relationship of these data with floral biology and breeding system, and morph ratio were evaluated. Pollen deposition and capture occurred in specific sites of the floral visitor body, showing the functionality of enantiostyly. The floral architecture, associated with the floral visitor behaviour, resulted in indirect pollen deposition on the floral visitor body. This occurred through a loop made by the pollen upon the inner petal surface, similar that generally reported for other Cassiinae. Chamaecrista ramosa is self-compatible, although no fruit set was observed through spontaneous self-pollination. The occurrence and number of floral morphs was similar within clumps. Enantiostyly seems to be advantageous for this species, as it results in efficient pollen capture and deposition, reduces the chances of autogamy and maximises intermorph pollen flow.

Why two kinds of stamens in buzz-pollinated flowers? Experimental support for Darwin’s division-of-labor hypothesis

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Full-text available

Oct 2008

1. Most animal-pollinated flowering plants offer nectar as a reward for their pollinators. Some 20 000 species, however, offer only pollen and rely on pollen-foraging bees for pollination. This creates a dilemma since pollen grains contain the male gametes and should be protected from becoming bee food. Darwin was the first to hypothesize that a 'division-of-labour' among stamens could solve this dilemma, with some stamens providing pollen as food, others providing pollen for fertilization. This hypothesis can only be tested if pollen grains from the two sets of stamens can be distinguished and their fates determined to the point of attachment on the stigma. 2. We tested Darwin's hypothesis in Melastoma malabathricum (Melastomataceae), a pollen-only flower with conspicuously differentiated stamens, an inner set that is short and yellow and an outer set that is much longer and purple with small yellow spurs. Pollen release is through terminal anther pores. Taking advantage of different exine patterns on the pollen produced by the two sets of stamens, we carried out a series of experimental manipulations to compare pollinator foraging behaviour and pollen pathways from anthers to stigmas. 3. The results demonstrate that in spite of all 10 stamens being buzzed simultaneously by the carpenter bees that pollinate M. malabathricum , pollen from the purple 'fertilization' stamens is dramatically more likely to land on stigmas than pollen from the yellow 'feeding' stamens. Removal experiments showed that the yellow 'feeding' stamens also attracted pollinators from a distance. Flowers that had their anther pores plugged received fewer buzzing bouts per visit, indicating that bees assessed the amount of pollen received per bout. Surprisingly, there was no significant difference in pollen loads on stigmas of flowers that had their anthers plugged and stigmas of controls, demonstrating the efficiency of vector-assisted cross-pollination and the lack of vector-assisted self-pollination. 4. The unexpectedly precise placement of pollen grains even with buzz pollination, with a large proportion of the grains deposited out of the bees' grooming reach, helps explain the evolutionary persistence of pollen as a reward in spite of the bees' ability to assess the amount of pollen received during foraging bouts. Together, these results strongly support Darwin's division-of-labour hypothesis.

Variation in pollinator effectiveness in swamp milkweed, Asclepias incarnata (Apocynaceae)

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Feb 2003

The contribution of a pollinator toward plant fitness (i.e., its "effectiveness") can determine its importance for the plant's evolutionary ecology. We compared pollinators in a population of Asclepias incarnata (Apocynaceae) for several components of pollinator effectiveness over two flowering seasons to evaluate their importance to plant reproduction. Insects of the order Hymenoptera predominate in A. incarnata pollination, but there appears to be no specialization for pollination within this order. Pollinators varied significantly in nearly every component of effectiveness that we measured, including pollen load, removal and deposition of pollen, pollination efficiency (deposition/removal), flower-handling time, and potential for geitonogamy (fractional pollen deposition). The visitation rate of pollinators also varied significantly between years and through time within years. Pollination success and percentage fruit-set of unmanipulated plants in the population also varied significantly between years, and pollination success varied among sample times within years. Most components of effectiveness were weakly correlated, suggesting that the contributions of visitor species toward pollination varied among effectiveness components. Mean flower-handling time, however, was strongly correlated with several components, including pollen removal and deposition, pollination efficiency, and fractional pollen deposition. These findings highlight the significance of pollination variability for plant reproduction and suggest that time-dependent foraging behaviors may play an important role in determining pollinator effectiveness.

Trait correlates and functional significance of heteranthery in flowering plants

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Oct 2010
NEW PHYTOL

• Flowering plants display extraordinary diversity in the morphology of male sexual organs, yet the functional significance of this variation is not well understood. Here, we conducted a comparative analysis of floral correlates of heteranthery - the morphological and functional differentiation of anthers within flowers - among angiosperm families to identify traits associated with this condition. • We performed a phylogenetic analysis of correlated evolution between heteranthery and several floral traits commonly reported from heterantherous taxa. In addition, we quantified the effect of phylogenetic uncertainty in the observed patterns of correlated evolution by comparing trees in which polytomous branches were randomly resolved. • Heteranthery is reported from 12 angiosperm orders and is phylogenetically associated with the absence of floral nectaries, buzz-pollination and enantiostyly (mirror-image flowers). These associations are robust to particularities of the underlying phylogenetic hypothesis. • Heteranthery has probably evolved as a result of pollinator-mediated selection and appears to function to reduce the conflict of relying on pollen both as food to attract pollinators and as the agent of male gamete transfer. The relative scarcity of heteranthery among angiosperm families suggests that the conditions permitting its evolution are not easily met despite the abundance of pollen-collecting bees and nectarless flowers.

Chamaecrista (Leguminosae) of the Diamantina Plateau, Minas Gerais, Brazil, with six new species and taxonomic novelties

Article

Oct 2020

Floras are still important for modern biodiversity studies, as they generate basic information, as well as improve understanding on the diversity of an area. This study aimed to the taxonomic study of the species of Chamaecrista from the Diamantina Plateau in Minas Gerais, Brazil, discussing morphological characteristics of the species and presenting taxonomic novelties. The work was based on the survey of herbaria collections, literature review and field expeditions. Descriptions, an identification key, illustrations of diagnostic features, photographic plates, and commentaries are presented for the 64 species of Chamaecrista from the Diamantina Plateau. Six new species are described, two lectotypifications (C. aurivilla and C. brachystachya) and one neotypification are made (C. echinocarpa), 11 new synonyms and taxonomic changes are proposed for C. astrochiton, C. claussenii, C. echinocarpa, C. exsudans, C. multipennis, and C. orbiculata. Chamaecrista sect. Xerocalyx is treated as a species complex with four taxa although more studies are needed to better understand this group.

Flowers with poricidal anthers and their complex interaction networks-Disentangling legitimate pollinators and illegitimate visitors

Article

Oct 2018

In flowers with poricidal anthers, pollen is not freely accessible and legitimate access is restricted to bees capable of vibrating the anthers. Despite the protection of pollen provided by poricidal anthers, numerous illegitimate, non‐buzz‐pollinating flower visitors rob pollen. We aimed to quantify the influence of functional groups of floral visitors and illegitimate interactions on the network structure to disentangle the flower visitor network into its mutualistic and antagonistic components. We delimited three functional groups of bees based on their pollen collection behaviour in poricidal flowers: large bees that vibrate entire flowers in a single buzzing position (flower buzzing), bees vibrating single anthers in different positions (anther buzzing) and non‐vibrating flower‐damaging or gleaning bees (non‐buzzing). Moreover, we characterized legitimate and illegitimate interactions of co‐occurring and co‐flowering plants and their flower visitors based on the stigma contact during a visit. Since we independently assessed the type of interaction with bee–plant species combinations, we were able to include the behavioural variations of each bee species across different flowers. The networks were modular, with stronger interactions within subsets of species than among the subsets. All modules included a combination of flower‐, anther‐ and non‐buzzing bees, and mutualistic and antagonistic networks were intermingled. Seven bee species shifted their roles across plant species. Specialization in the subset of interactions with pollinators was higher than the overall visitation network. Flower‐buzzing bees were more specialized than anther‐buzzing and non‐buzzing bees, which used virtually all poricidal flowers similarly. Although plants with poricidal anthers shared a specialized mechanism of pollen release, their pollinators were highly dissimilar and formed compartments of interacting species. The interaction‐level approach taken in our study confers a high specificity to the pollinator network, leading to a more complex and realistic picture of mutualistic webs versus its embedded florivory, which are otherwise confounded in pooled networks across flower visitors. A plain language summary is available for this article.

Relationship of floral morphology and development with the pattern of bee visitation in a species with pollen-flowers, Chamaecrista desvauxii (Fabaceae)

Article

Apr 2018

Chamaecrista exhibits a suite of floral traits associated with buzz pollination, and its morphology and organogenesis play crucial roles in pollination because bees can exploit anthers at distinct developmental stages. Here we investigated the relationship of floral morphology and development with the bee visitation pattern in Chamaecrista desvauxii var. latistipula. We also explored pollen structure, germination and stigma receptivity. Sepal growth was initially rapid and gradually slowed down as growth of the inner whorls accelerated. Heteranthery arose early during flower development and was not accompanied by morphological or histochemical differences in pollen grains, suggesting that stamen differentiation in the context of the 'division-of-labour' hypothesis was in no way associated with pollen differences. The stigma was receptive and pollen grains from both anther morphs were viable before anthesis. Bee species showed specific behaviours on anthers at both flower stages, from chewing to buzzing, in some cases touching the stigmatic region during pollen collection. Pollination experiments indicated similar fruit set between anthetic flowers and pre-anthetic buds, suggesting that pollination could occur before anthesis, even though floral buds have distinct whorl arrangements. This study highlights the existence of an extended window of opportunity for mutualistic interactions between bees and flowers in a typical species of Fabaceae with pollen-flowers. ADDITIONAL KEYWORDS: Brazil-flower development-Leguminosae-pollen grains-pollination ecology-pollinator behaviour.

Buzz‐pollination in Neotropical bees: Genus‐dependent frequencies and lack of optimal frequency for pollen release

Article

Jun 2018

Over 50 genera of bees release pollen from flower anthers using thoracic vibrations, a phenomenon known as buzz-pollination. The efficiency of this process is directly affected by the mechanical properties of the buzzes, namely the duration, amplitude, and frequency. Nonetheless, although the effects of the former two properties are well described, the role of buzz frequency on pollen release remains unclear. Furthermore, nearly all of the existing studies describing vibrational properties of natural buzz-pollination are limited to bumblebees (Bombus) and carpenter bees (Xylocopa) constraining our current understanding of this behavior and its evolution. Therefore, we attempted to minimize this shortcoming by testing whether flower anthers exhibit optimal frequency for pollen release and whether bees tune their buzzes to match these (optimal) frequencies. If true, certain frequencies will trigger more pollen release and lighter bees will reach buzz frequencies closer to this optimum to compensate their smaller buzz amplitudes. Two strategies were used to test these hypotheses: (i) the use of (artificial) vibrational playbacks in a broad range of buzz frequencies and amplitudes to assess pollen release by tomato plants (Solanum lycopersicum L.) and (ii) the recording of natural buzzes of Neotropical bees visiting tomato plants during pollination. The playback experiment indicates that although buzz frequency does affect pollen release, no optimal frequency exists for that. In addition, the recorded results of natural buzz-pollination reveal that buzz frequencies vary with bee genera and are not correlated with body size. Therefore, neither bees nor plants are tuned to optimal pollen release frequencies. Bee frequency of buzz-pollination is a likely consequence of the insect flight machinery adapted to reach higher accelerations, while flower plant response to buzz-pollination is the likely result of its pollen granular properties.

The stigmatic orifice in Cassia , Senna , and Chamaecrista (Caesalpiniaceae): morphological variation, function during pollination, and possible adaptive significance

Article

Nov 1994

In species of Cassia, Senna, and Chamaecrista an orifice leading into a stigmatic cavity is present at the tip of the style. The size of the orifice, the occurrence and morphology of surrounding trichomes or papillae, and the occurrence of a drop of secretion at its outlet were recorded in 17 species belonging to the three genera of the subtribe Cassiinae. Much of the observed variation in these characters apparently reflects different modes of pollen capturing and varying degrees of secretion exposure. In some of the species studied no secretion was noticeable at the entrance to the stigmatic cavity. The unusual type of stigma in the Cassiinae does not fit into any of the recognized main groups of angiosperm stigmas. It is conjectured that in the buzz-pollinated Cassiinae species with small stigmatic orifices, the secretory material is retained within the stigmatic cavity, to be extruded by vibratory movements of the style induced by a buzzing bee. It is also hypothesized that in the wet tropics, concealment of secretory materials within a cavity prevents their washing away or dilution by rain. Furthermore, in the Cassiinae, the considerable variation in features of the style and of the stigma may function as mechanisms isolating between sympatric, visitor-sharing, concurrently blooming species.

Constant flower damage caused by a common stingless bee puts survival of a threatened buzz-pollinated species at risk

Article

Oct 2017

Illegitimate flower visitors may reduce the reproductive success of their host plants. Eriocnema fulva, a threatened Melastomataceae of the Atlantic Forest, Brazil, has pollen flowers with poricidal anthers that show frequent damage of floral parts. We identified the flower-damaging bees and determined their impact on fruit set. Bees of seven species visited their flowers, but only three species collected pollen by vibration. With only one visit to a flower patch per 12 h, the frequency of effective buzz pollinating bees was negligible, while flower-damaging workers of the stingless bee Trigona fulviventris (Apidae) accounted for 70% of the visits. During their lengthy visits, they cut anthers to access pollen, and often styles as well. We conclude that the direct negative consequence of flower damage by Trigona bees, as well as their indirect impact by making the flowers unattractive for effective pollinators is a major reason for the low fruit set (6.9%) of E. fulva. Considering the rareness of the plant species, these negative effects put the survival of E. fulva at risk.

Heteranthery as a solution to the demand for pollen as food and for pollination - Legitimate flower visitors reject flowers without feeding anthers

Article

Aug 2017
PLANT BIOLOGY

Heteranthery, the presence of feeding and pollinating anthers in the same flower, seems to mediate the evolutionary dilemma for plants to protect their gametes and yet provide food for pollinators. This study aims to elucidate the role of heteranthery in the buzz-pollinated Senna reniformis. The fecundity of pollen from long, medium and short-sized anthers was determined by hand cross-pollination experiments, and the quantity, size, ornamentation and viability of pollen of different anthers were compared. Rates of flower rejection by bees were measured in anther removal experiments to assess the preferences of flower visitors for feeding or pollinating anthers. Large bees, which were the effective pollinators of self-incompatible S. reniformis, avoided flowers without short feeding anthers, but not those without medium or long anthers. Illegitimate small and medium-sized bees were unresponsive to anther exclusion experiments. Long anthers deposited pollen on the back and short anthers on the venter of large bees. Pollen from long anthers had higher in vitro viability and higher fruit and seed set after cross-pollination than pollen from other sized anthers. Short anthers produce feeding pollen to effective pollinators and long anthers are related to pollination of S. reniformis. Bee behaviour and size was found to directly influence the role of anthers in the “division of labour”. Only large bee pollinators that carry the pollinating pollen from long anthers in “safe sites” associated short anthers with the presence of food. In the absence of these larger bee pollinators, the role of heteranthery in S. reniformis would be strongly compromised and its function would be lost.

Ricochet pollination in Senna (Fabaceae) − petals deflect pollen jets and promote division of labour among flower organs

Article

Jul 2017
PLANT BIOLOGY

Naturalists Fritz and Hermann Müller hypothesised that heteranthery often leads to a division of labour into ‘feeding’ and ‘pollinating’ stamens; the latter often being as long as the pistil so as to promote successful pollination on the bees’ back. In many buzz‐pollinated species of Senna , however, the so‐called pollinating stamens are short and not level with the stigma, raising the question of how pollen is shed on the bees’ back. Here we explore a mechanism called ‘ricochet pollination’. We test whether division of labour is achieved through the interaction between short lower stamens and strongly concave ‘deflector petals’. We studied the arrangement and morphology of the floral organs involved in the ricochet pollination, functioning of the flowers through artificial sonication and observed the interactions between bees and flowers in the field. The middle stamens are adapted to eject pollen downwards, which can be readily collected on the bee mid legs. Most of the pollen is ejected towards the deflector petal(s). Pollen from this set of stamens is more likely to contribute to pollination. The pollen grains seem to ricochet multiple times against the deflector petals to eventually reach the bee's back. The pollen ricochet mechanism promotes a division of labour by involving additional floral organs, such as petals, reinforcing the Müllers’ division‐of‐labour hypothesis. However, alternative, non‐multiexclusive hypotheses could be explored in genus Senna and other angiosperm species.

R: A Language and Environment for Statistical Computing

Book

Jan 2015

Core R Team

Buzz pollination of Cassia quiedondilla (Leguminosae) by bees of the genera Centris and Melipona

Article

Jan 1974

Stephen Buchmann

Buzz pollination in angiosperms

Article

Jan 1983

Stephen Buchmann

An interesting method of pollen collecting by bees from flowers with tubular anthers

Article

Jan 1962

C.D. Michener

Intra-specific body size determines pollination effectiveness

Article

Dec 2016
BASIC APPL ECOL

Pollinators differ in morphological and behavioral traits. The effect of the resulting trait variation on pollination effectiveness at the level of different species has received considerable attention, while the effect of intra-specific trait variation at the population level is largely unexplored. We examined the impact of body size variation in the Red Mason bee Osmia rufa on the yield of oilseed rape in a caged field experiment. Crop yield was positively correlated to mean individual body size. Comparison with control plots showed that only large individuals increased yield to a level above pollinator-free variation. Small individuals, in contrast, even decreased yield compared to the variation within controls. Thus, the fitness of pollinator populations significantly affects pollination services, because adult body size is determined by the resource availability at the larval stage. Our results emphasize the need for complementing investigations on pollinator communities by analysis of the individual species involved. We conclude that only the availability of sufficient floral resources enables wild bee foragers to produce large, persistent offspring constituting effective pollinators for sustainable pollination services in the following season

The screening game in plant–pollinator interactions

Article

Jul 2015

A central question in the field of plant-pollinator interactions is whether and how can plants choose the optimal pollinators when plants cannot directly assess the quality of floral visitors. To answer this question and to provide a new perspective to this problem, we develop a screening game modeling the plant-pollinator interaction. We propose that some floral traits could be interpreted as an entry barrier with a strategic cost the plants impose on floral visitors. The pollinators decide to further interact with the plant only if the cost is not prohibitive. Therefore, by imposing the right level of costs, the plants may achieve interactions only with high-quality pollinators without a priori knowing the quality of visitors.

The Functional Significance of Poricidal Anthers and Buzz Pollination: Controlled Pollen Removal From Dodecatheon

Article

Aug 1994

1. Given the diminishing returns associated with animal pollination, floral mechanisms that restrict pollen removal by individual pollinators and encourage transport on many pollinators generally promote a plant's cumulative success in pollen dispersal. Effective mechanisms for dispensing pollen should allow facultative adjustment of removal in response to the prevailing frequency of visits to a plant. 2. We investigated whether the poricidal anthers of Dodecatheon conjugens, a buzz-pollinated species, function as dispensing mechanisms by (a) comparing pollen removal in response to buzz frequencies that pollen-collecting bumble-bees (Bombus spp.) produce (≤400 Hz) with removal stimulated by higher frequencies and (b) comparing removal from flowers that waited different periods of time for their first visit. 3. Mechanical vibration of D. conjugens flowers for 1s at frequencies ≤400 Hz removed an average of 9.7% of available pollen, compared to 23.4% for 450-1000 Hz vibrations (all frequencies involved similar input energy). Buzzing by bees and mechanical vibration removed more pollen from older virgin flowers. 4. These results imply that the poricidal anthers of Dodecatheon flowers are `tuned' higher than the buzz frequencies used by their pollen-collecting pollinators, so that they effectively restrict pollen removal, while also allowing increased removal when visits occur rarely. Previously published results from other buzz-pollinated species indicate that poricidal anthers generally function as dispensing mechanisms. 5. Poricidal anthers probably enabled convergent evolution of the solanoid flower, which localizes pollinator-flower contact so as to reduce pollen loss during transport.

The Widespread Occurrence of Anther Destruction by Trigona Bees in Melastomataceae

Article

Dec 1983

Susanne Renner

A complex behavior pattern of pollen robbing by several species of the large tropical bee genus Trigona (Apidae: Meliponinae, tribe Trigonini) is described. These bees probe pollen from the apical pores of tubular Melastomataceae anthers as far as their tongues reach and then cut off the top of the anther to expose more pollen. This is repeated several times. A summary of observations of this syndrome in 34 species of Brazilian Melastomataceae and records from other neotropical countries are presented. The significance of these pollen robbers' adaptations is examined.

The Breeding System and Pollinators of Melastoma affine (Melastomataceae); A Pioneer Shrub in Tropical Australia

Article

Dec 1993

C. L. Gross

Melastoma affine D. Don. (Melastomataceae) is a pioneer species of rain forest and wet-sclerophyll habitats in the Australasian region. The breeding system and pollen vectors of Melastoma affine in the Mt. Spec region, North Queensland, were investigated over two seasons. Melastoma affine is self-compatible but does not produce fruit via autogamy or apomixis, i.e., pollen vectors are required for fruit set. The colonizing success of this species is thus dependent on the presence of a pollinator population. Eight bee species were commonly recorded at the nectar-less flowers of M. affine; although only Lestis bombylans, Nomia sp., Amegilla anomola, and Xylocopa near gressitti consistently contacted the stigma during foraging. When sunny weather prevails natural fruit set in M. affine reaches 90 percent, reflecting high visitation and subsequent pollination by such pollinators. The dimorphic stamens of M. affine both contain viable pollen which has to be extracted from an apical pore. Two modes of pollen extraction were common: buzz pollen collection, where pollen is vibrated from anthers; and, anther destruction, where pollen is removed from holes made by bees. Pollen collectors that buzz anthers spend less time at flowers than bees that extract pollen by other means. Furthermore, bees that gather pollen via destructive means rarely touch melastome stigmas.

Assessment of pollen reward and pollen availability in Solanum stramoniifolium and Solanum paniculatum for buzz-pollinating carpenter bees

Article

Oct 2013
PLANT BIOLOGY

The two widespread tropical Solanum species S. paniculatum and S. stramoniifolium are highly dependent on the visits of large bees that pollinate the flowers while buzzing them. Both Solanum species do not offer nectar reward; the rewarding of bees is thus solely dependent on the availability of pollen. Flower visitors are unable to visually assess the amount of pollen, because the pollen is hidden in poricidal anthers. In this study we ask whether and how the amount of pollen determines the attractiveness of flowers for bees. The number of pollen grains in anthers of S. stramoniifolium was seven times higher than in S. paniculatum. By contrast, the handling time per five flowers for carpenter bees visiting S. paniculatum was 3.5 times shorter than of those visiting S. stramoniifolium. As a result foraging carpenter bees collected a similar number of pollen grains per unit time on flowers of both species. Experimental manipulation of pollen availability by gluing the anther pores showed that the carpenter bees were unable to detect the availability of pollen by means of chemical cues before landing and without buzzing. Our study shows that the efficiency of pollen collecting on S. paniculatum is based on large inflorescences with short between-flower search times and short handling time of individual flowers, whereas that of S. stramoniifolium relies on a large amount of pollen per flower. Interestingly, large carpenter bees are able to adjust their foraging behaviour to drastically different strategies of pollen reward in otherwise very similar plant species.

Pollinator abundance and behavior on Aconitum lycoctonum (Ranunculaceae): An analysis of the quantity and quality components of pollination

Article

Jun 2000
OIKOS

The yellow-flowered monkshood Aconitum lycoctonum has variable degrees of inbreeding among populations, despite being primarily bee-pollinated. Here we examined the pollination ecology of A. lycoctonum. We investigated pollinator community and frequency in four populations at two altitudes over two years. We found that flowers were more often visited at low elevation than at high elevation. However, because flowers lived longer at high elevation than at low elevation, and plants at high elevation had more flowers than at low elevation, the overall chance of a plant being visited may be greater at high elevation. Breeding system experiments showed that at least some populations of A. lycoctonum were self-compatible and also were not completely protandrous. Thus selfing, especially by geitonogamous pollen, will be common if pollinators often visit several flowers within a plant, as we found to be true for the main pollinator (bumblebees) of A. lycoctonum. Although the stereotypical behavior of bees is to move upwards, 17% of the within-plant movements of the main pollinator (Bombus gerstaeckeri) were downwards, i.e. from a male-phased to a female-phased flower because the flowers open from the bottom to the top of the plant. Other pollinators of A. lycoctonum moved less often within plants. We conclude that in addition to differences in self-compatibility, differences in pollinator abundance and behavior could have led to variation in the realized mating system in different A. lycoctonum populations.

The Stigmatic Orifice in Cassia, Senna, and Chamaecrista (Caesalpiniaceae): Morphological Variation, Function During Pollination, and Possible Adaptive Significance

Article

Nov 1994

What's the ‘buzz’ about? The ecology and evolutionary significance of buzz-pollination

Article

Jun 2013

The ecology of pollen limitation in buzz-pollinated Rhexia virginica (Melastomataceae)

Article

Dec 2001
J ECOL

1 Pollen limitation of female fertility has often been documented in animal‐pollinated plants, but seldom have the ecological mechanisms responsible been investigated. We examined factors influencing pollen limitation in Rhexia virginica (Melastomataceae), a species in which pollen transfer depends on bumblebees capable of buzz pollination. Experimental studies were conducted in two populations at Lake Matchedash, southern Ontario, Canada, where the species occurs at the edge of its familial range. 2 Supplemental hand pollination of flowers increased their probability of fruit set compared with open‐pollinated control flowers by an average of 57.6%. Pollen limitation was assessed on a per flower basis because the median floral display size at Lake Matchedash was one flower. Pollen limitation was prevalent throughout the 3–4‐week blooming period in one population, whereas in the other it was only evident at the beginning of flowering, despite their close proximity. 3 Bumblebee visits (primarily Bombus impatiens ) to R. virginica flowers were infrequent and variable in their occurrence. Visitation was recorded on 14 days during flowering. The median number of visits was 0.65 bees per hour; on 6 days there was virtually no bee activity, but on 2 days visitation rates were high. Variation in pollinator activity was apparently unrelated to local weather conditions. 4 Field experiments demonstrated that the poricidal anthers of R. virginica dispense pollen gradually, with only 10.2% of pollen removed from flowers during a single bumblebee visit. This level of pollen removal is lower than reported in other flowering plants. On average, 47.3% of pollen remained in anthers at the end of anthesis. 5 Investigation of the relation between pollen dispersal and pollen limitation demonstrated a significant negative correlation between the proportion of pollen removed from anthers on a given day and the intensity of pollen limitation. It appears that the pollen‐dispensing mechanism of R. virginica and infrequent visitation by bumblebees compromise pollen dispersal, causing pollen limitation in Ontario populations.

Bees assess pollen returns while sonicating Solanum flowers

Article

Jan 1989

Can bees accurately gauge accumulating bodily pollen as they harvest pollen from flowers? Several recent reports conclude that bees fail to assess pollen harvest rates when foraging for nectar and pollen. A native nightshade (Solanum elaeagnifolium Cavanilles) that is visited exclusively for pollen by both solitary and social bees (eg. Ptiloglossa and Bombus) was studied in SE Arizona and SW New Mexico. The flowers have no nectaries. Two experiments were deployed that eliminated pollen feedback to the bees by experimentally manipulating flowers prior to bee visits. The two methods were 1) plugging poricidal anthers with glue and 2) emptying anthers of pollen by vibration prior to bee visitation. Both experiments demonstrated that bees directly assess pollen harvest on a flower-by-flower basis, and significantly tailor their handling times, number of vibratile buzzes per flower and grooming bouts according to the ongoing harvest on a given flower. In comparison to experimental flowers, floral handling times were extended for both Bombus and Ptiloglossa on virgin flowers. Greater numbers of intrafloral buzzes and numbers of times bees groomed pollen and packed it into their scopae while still on the flower were also more frequent at virgin versus experimental flowers. Flowers with glued andreocia received uniformly brief visits from Bombus and Ptiloglossa with fewer sonications and virtually no bouts of grooming. Curtailed handling with few buzzes and grooms also characterized visits to our manually harvested flowers wherein pollen was artificially depleted. Sonicating bees respond positively to pollen-feedback while harvesting from individual flowers, and therefore we expect them to adjust their harvesting tempo according to the currency of available pollen (standing crop) within Solanum floral patches.

Anther and stigma morphology in mirror-image flowers of Chamaecrista chamaecristoides (Fabaceae): Implications for buzz pollination

Article

Jan 2011
PLANT BIOLOGY

Enantiostyly (mirror-image flowers) is usually associated with buzz pollination. In buzz-pollinated flowers, pollen is released through terminal pores after bees vibrate the stamens. Several studies have evaluated the function of 'buzzing' in pollen release, but less attention has been paid to the effect of buzzing on pollen capture and deposition on stigmas. Evaluating the mechanism of pollen dispersion in buzz-pollinated flowers is important because it may affect mating patterns and reproductive success. In this study, we analysed the morphology of sexual organs (anther and stigma) using electron microscopy, and determined the relationship between sexual organ structure and pollen capture function through experimental manipulations of buzz-pollinated flowers of Chamaecrista chamaecristoides, as well as vibration frequencies on floral visitors. Pollen release occurs through two terminal pores at the tip of the stamens. However, unlike most angiosperms that have their stigmatic surface exposed, C. chamaecristoides presents a stigmatic surface inside a cavity covered by trichomes. Experimental manipulations showed that effective fertilisation is only achieved when the style is vibrated, suggesting that buzzing is not only important for pollen release but also for pollen capture and deposition on the stigma. This result, in addition to vibration frequency analysis, suggests that although all floral visitors buzz flowers only those that buzz at higher frequencies achieve effective fertilisation. The anatomical features of sexual organs in flowers of C. chamaecristoides demonstrate that this species possesses a highly specialised, elaborate morphology, with both genders selected for traits that promote buzz pollination.

The Ecology and Natural History of Tropical Bees

Article

Sep 1989

David Roubik

Preface Acknowledgments Part I. Introduction: 1. Approaches to tropical bee biology 2. Diversity of tropical bees Part II. Foraging and Pollination: 3. Resources gathered by bees 4. Mechanisms of resource collection 5. Foraging and flight activity 6. Pollination ecology Part III. Nesting and Reproduction Biology: 7. Bee nests 8. Nest predators, associates and defense 9. Mating and brood production Part IV. Community Ecology: 10. Seasonality, abundance and flower preference 11. Composition of bee assemblages 12. Roles of bees in communities References Index Appendices.

Minimum size threshold of visiting bees of a buzz‐pollinated plant species: consequences for pollination efficiency

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