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.

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.

Global patterns and drivers of buzzing bees and poricidal plants.

Foraging behavior frequently plays a major role in driving the geographic distribution of animals. Buzzing to extract protein-rich pollen from flowers is a key foraging behavior used by bee species across at least 83 genera (these genera comprise ∼58% of all bee species). Although buzzing is widely recognized to affect the ecology and evolution of bees and flowering plants (e.g., buzz-pollinated flowers), global patterns and drivers of buzzing bee biogeography remain unexplored. Here, we investigate the global species distribution patterns within each bee family and how patterns and drivers differ with respect to buzzing bee species. We found that both distributional patterns and drivers of richness typically differed for buzzing species compared with hotspots for all bee species and when grouped by family. A major predictor of the distribution, but not species richness overall for buzzing members of four of the five major bee families included in analyses (Andrenidae, Halictidae, Colletidae, and to a lesser extent, Apidae), was the richness of poricidal flowering plant species, which depend on buzzing bees for pollination. Because poricidal plant richness was highest in areas with low wind and high aridity, we discuss how global hotspots of buzzing bee biodiversity are likely influenced by both biogeographic factors and plant host availability. Although we explored global patterns with state-level data, higher-resolution work is needed to explore local-level drivers of patterns. From a global perspective, buzz-pollinated plants clearly play a greater role in the ecology and evolution of buzzing bees than previously predicted.

Biomechanical properties of non-flight vibrations produced by bees.

Bees use thoracic vibrations produced by their indirect flight muscles for powering wingbeats in flight, but also during mating, pollination, defence and nest building. Previous work on non-flight vibrations has mostly focused on acoustic (airborne vibrations) and spectral properties (frequency domain). However, mechanical properties such as the vibration's acceleration amplitude are important in some behaviours, e.g. during buzz pollination, where higher amplitude vibrations remove more pollen from flowers. Bee vibrations have been studied in only a handful of species and we know very little about how they vary among species. In this study, we conducted the largest survey to date of the biomechanical properties of non-flight bee buzzes. We focused on defence buzzes as they can be induced experimentally and provide a common currency to compare among taxa. We analysed 15,000 buzzes produced by 306 individuals in 65 species and six families from Mexico, Scotland and Australia. We found a strong association between body size and the acceleration amplitude of bee buzzes. Comparison of genera that buzz-pollinate and those that do not suggests that buzz-pollinating bees produce vibrations with higher acceleration amplitude. We found no relationship between bee size and the fundamental frequency of defence buzzes. Although our results suggest that body size is a major determinant of the amplitude of non-flight vibrations, we also observed considerable variation in vibration properties among bees of equivalent size and even within individuals. Both morphology and behaviour thus affect the biomechanical properties of non-flight buzzes.

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

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 synthesize 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.

Plant Resource Use and Pattern of Usage by the Naturalized Orchid Bee (Euglossa dilemma: Hymenoptera: Apidae) in Florida.

The Neotropical orchid bee Euglossa dilemma was found to be naturalized in southern Florida in 2003, and, by 2022, it had colonized the southern half of Florida. Observations of the bee's collection of plant resources, primarily flowers, were made from 2003 through to 2022 to document its plant usage and understand the patterns of its plant usage. The bee utilized 259 plant taxa, 237 species, and 22 horticultural forms, in 156 genera and 56 families in 263 total uses. Of 247 taxa of flowers, 120 were visited primarily for nectar, 46 for both nectar and pollen, 60 for pollen, including 42 buzz-pollinated flowers, 15 for fragrance chemicals for the males, and 5 for resin rewards by females for nesting. Fragrance chemicals were also collected by males from the leaves of 12 plant species. These extensive resource use data allowed the following predictions to be made. (1) The bee's presence in Florida, distant from its native region of Mexico and Central America and the geographical ranges of other orchid bees, would result the usage of many new taxa of plants. True, half, 74/148 (50%), of the genera and one third, 16/51(31%), of the plant families of the plants with flowers used by the bee were not previously recorded as being utilized by Euglossine bees. (2) Like other naturalized bees, it would use relatively more plants from its native range or congeners of these plants. True, 113/148 (76%) of genera with species bearing collected floral rewards are native or congeners with species native to the bee's native range. (3) Given the bee's long tongue, ability to buzz pollen from poricidal anthers, and ability to collect and use specialized rewards, it would disproportionately use plants with protected or highly specialized floral rewards. True, 180/247 (72%) utilized species bear rewards which were protected and unavailable to, or of no interest to, most other flower visitors.

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

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.

Heteromorphic stamens are differentially attractive in Swartzia (Fabaceae).

The division of labour 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 centre 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 odour 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.

Floral orientation affects outcross-pollen deposition in buzz-pollinated flowers with bilateral symmetry.

PREMISE: Floral orientation is central to plant-pollinator interactions and is commonly associated with floral symmetry. Bilaterally symmetrical flowers are often oriented horizontally for optimal pollinator positioning and pollen transfer efficiency, while the orientation of radially symmetrical flowers is variable. Buzz-pollinated species (pollinated by vibration-producing bees) include bilateral, horizontally oriented flowers, and radial, pendant flowers. The effect of floral orientation on pollen transfer has never been tested in buzz-pollinated species. METHODS: Here, we examined the effect of floral orientation on bumblebee-mediated pollen deposition in three buzz-pollinated Solanum species with different floral symmetry and natural orientations: S. lycopersicum and S. seaforthianum (radial, pendant), and S. rostratum (bilateral, horizontal). We tested whether orientation affects total stigmatic pollen deposition (both self and outcross pollen) when all flowers have the same orientation (either pendant or horizontal). In a second experiment, we evaluated whether different orientations of donor and recipient flowers affects the receipt of outcross pollen by S. rostratum. RESULTS: For the three Solanum species studied, there was no effect of floral orientation on total pollen deposition (both self and outcross) when flowers shared the same orientation. In contrast, in our experiment with S. rostratum, we found that pendant flowers received fewer outcross-pollen grains when paired with pendant donors. CONCLUSIONS: We suggest that floral orientation influences the quality of pollen transferred, with more outcross pollen transferred to horizontally oriented recipients in the bilaterally symmetrical S. rostratum. Whether other bilaterally symmetrical, buzz-pollinated flowers also benefit from increased cross-pollination when presented horizontally remains to be established.

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

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.

Structural dynamics of real and modelled Solanum stamens: implications for pollen ejection by buzzing bees.

An estimated 10% of flowering plant species conceal their pollen within tube-like anthers that dehisce through small apical pores (poricidal anthers). Bees extract pollen from poricidal anthers through a complex motor routine called floral buzzing, whereby the bee applies vibratory forces to the flower stamen by rapidly contracting its flight muscles. The resulting deformation depends on the stamen's natural frequencies and vibration mode shapes, yet for most poricidal species, these properties have not been sufficiently characterized. We performed experimental modal analysis on Solanum elaeagnifolium stamens to quantify their natural frequencies and vibration modes. Based on morphometric and dynamic measurements, we developed a finite-element model of the stamen to identify how variable material properties, geometry and bee weight could affect its dynamics. In general, stamen natural frequencies fell outside the reported floral buzzing range, and variations in stamen geometry and material properties were unlikely to bring natural frequencies within this range. However, inclusion of bee mass reduced natural frequencies to within the floral buzzing frequency range and gave rise to an axial-bending vibration mode. We hypothesize that floral buzzing bees exploit the large vibration amplification factor of this mode to increase anther deformation, which may facilitate pollen ejection.

Anther cones increase pollen release in buzz-pollinated Solanum flowers.

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 bioadhesives 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 characterized vibrations transmitted to other anthers and the amount of pollen released. We found that joined anther architectures cause nonfocal anthers to vibrate at higher amplitudes than free architectures. Moreover, in the two species with naturally loosely held anthers, anther fusion increases pollen release, whereas 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.

How and why do bees buzz? Implications for buzz pollination.

Buzz pollination encompasses the evolutionary convergence of specialized floral morphologies and pollinator behaviour in which bees use vibrations (floral buzzes) to remove pollen. Floral buzzes are one of several types of vibrations produced by bees using their thoracic muscles. Here I review how bees can produce these different types of vibrations and discuss the implications of this mechanistic understanding for buzz pollination. I propose that bee buzzes can be categorized according to their mode of production and deployment into: (i) thermogenic, which generate heat with little mechanical vibration; (ii) flight buzzes which, combined with wing deployment and thoracic vibration, power flight; and (iii) non-flight buzzes in which the thorax vibrates but the wings remain mostly folded, and include floral, defence, mating, communication, and nest-building buzzes. I hypothesize that the characteristics of non-flight buzzes, including floral buzzes, can be modulated by bees via modification of the biomechanical properties of the thorax through activity of auxiliary muscles, changing the rate of activation of the indirect flight muscles, and modifying flower handling behaviours. Thus, bees should be able to fine-tune mechanical properties of their floral vibrations, including frequency and amplitude, depending on flower characteristics and pollen availability to optimize energy use and pollen collection.

Examining the Role of Buzzing Time and Acoustics on Pollen Extraction of Solanum elaeagnifolium.

Buzz pollination is a specialized pollination syndrome that requires vibrational energy to extract concealed pollen grains from poricidal anthers. Although a large body of work has examined the ecology of buzz pollination, whether acoustic properties of buzz pollinators affect pollen extraction is less understood, especially in weeds and invasive species. We examined the pollination biology of Silverleaf nightshade (Solanum elaeagnifolium), a worldwide invasive weed, in its native range in the Lower Rio Grande Valley (LRGV) in south Texas. Over two years, we documented the floral visitors on S. elaeagnifolium, their acoustic parameters (buzzing amplitude, frequency, and duration of buzzing) and estimated the effects of the latter two factors on pollen extraction. We found five major bee genera: Exomalopsis, Halictus, Megachile, Bombus, and Xylocopa, as the most common floral visitors on S. elaeagnifolium in the LRGV. Bee genera varied in their duration of total buzzing time, duration of each visit, and mass. While we did not find any significant differences in buzzing frequency among different genera, an artificial pollen collection experiment using an electric toothbrush showed that the amount of pollen extracted is significantly affected by the duration of buzzing. We conclude that regardless of buzzing frequency, buzzing duration is the most critical factor in pollen removal in this species.

Differential reward in "male" versus "female" pollen of functionally dioecious Solanum.

PREMISE: Five to six percent of angiosperm species exhibit a dioecious sexual system, with unisexual "male" or "female" flowers borne on separate plants. The consequent need for inter-individual pollen exchange is a special challenge for taxa where pollen is the sole pollinator reward. Dioecious Australian Solanum assure visits from pollen-foraging bees via production of inaperturate pollen in functionally female (morphologically bisexual) flowers. Biochemical composition of pollen from Australian Solanum has not been assessed nor compared to porate pollen from staminate flowers to reveal whether these flowers differ in their pollinator reward potential. METHODS: Porate pollen from male flowers and inaperturate pollen from functionally female flowers of two functionally dioecious Australian species were compared for protein and amino acid content. We also assessed pollen from bisexual and staminate flowers of a closely related andromonoecious species, in which all pollen is porate, as a comparison across co-occurring sexual systems. RESULTS: In both functionally dioecious species, porate pollen grains from staminate flowers had significantly higher levels of proteins and amino acids than inaperturate pollen grains from functionally female flowers. Levels of proteins and amino acids were highest in bisexual and staminate flowers of the andromonoecious species. CONCLUSIONS: Higher levels of proteins and amino acids in porate pollen of "male" flowers in our functionally dioecious Solanum species suggests a greater nutritive reward for bees foraging on "male" plants than for those foraging on functionally "female" plants. Greater reward in porate pollen (including andromonoecious species) may be connected to the potential to generate a pollen tube.

The predictive power of pollination syndromes: Passerine pollination in heterantherous Meriania macrophylla (Benth.) Triana (Melastomataceae).

The cloud forest species Meriania macrophylla (Benth.) Triana has pseudocampanulate flowers with bulbous stamen appendages, typical for the passerine pollination syndrome found in the Melastomataceae tribe Merianieae. The species is further characterized by strong stamen dimorphism (heteranthery), a condition otherwise associated with pollen-rewarding bee-pollinated species (both in Melastomataceae and beyond). In passerine-pollinated Merianieae, however, flowers usually only show weak stamen dimorphism. Here, we conducted field and laboratory investigations to determine the pollinators of M. macrophylla and assess the potential role of strong heteranthery in this species. Our field observations in Costa Rica confirmed syndrome predictions and indeed proved pollination by passerine birds in M. macrophylla. The large bulbous set of stamens functions as a food-body reward to the pollinating birds, and as trigger for pollen release (bellows mechanism) as typical for the passerine syndrome in Merianieae. In contrast to other passerine-pollinated Merianieae, the second set of stamens has seemingly lost its rewarding and pollination function, however. Our results demonstrate the utility of the pollination syndrome concept even in light of potentially misleading traits such as strong heteranthery.

La especie de bosque nuboso Meriania macrophylla (Benth.) Triana presenta flores pseudocampanuladas con estambres con un apéndice bulboso, una morfología típica de las flores polinizadas por aves paserinas en Merianieae. Además, la especie se caracteriza por tener dos verticilos diferentes de estambres (heteroanteria), una condición que generalmente se asocia a especies polinizadas por abejas con polen como recompensa. En las especies de Merianieae polinizadas por aves la heteroantería es leve, si presente. Para este estudio determinamos los polinizadores de M. macrophylla y evaluamos posibles explicaciones de la presencia de estambres heteroantéricos Nuestras observaciones de campo en Costa Rica confimaron nuestras predicciones de que la polinización de esta especie se da por aves. Los conectivos engrosados funcionan como recompensa para las aves, que al removerlos de la flor activan el mecanismo de expulsión de polen. En contraste, el segundo verticilo de estambres aparentemente perdió tanto la función de recompensa como su función reproductiva. Nuestros resultados demuestran la utilidad de los síndromes de polinización incluso en presencia de caracteres confusos como la presencia de heteroanteria muy marcada.

A sophisticated case of division of labour in the trimorphic stamens of the Cassia fistula (Leguminosae) flower.

Buzz-pollinated pollen flowers have pollen as the primary resource for pollinators and must deal with a conflict between the exploitation of pollen grains by bees and pollination success. It has been hypothesized that heterostemony allows division of labour between stamens as a solution to the pollen dilemma. To test the division of labour hypothesis, we chose Cassia fistula, which has a trimorphic androecium and analysed androecium development, pollen grain release mechanisms and visitor behaviour. We explored the reflectance of floral organs and carried out an exclusion experiment to test the attractiveness of each stamen morph to the bee species. Finally, we explored the structural, ultrastructural and functional variation between the pollen grains, including pollen viability across stamen morphs. The differences among the three stamen morphs, which is developed from two whorls of the stamen, are the first evidence of the division of labour in our study system. Large Bombus and Xylocopa bees actively and exclusively exploited the pollen grains from the central poricidal anthers generating pollen deposition on their bodies. The reflectance pattern of floral organs indicated a targeting of these large bees to the central anthers, corroborated by the anther manipulative experiment where only the exclusion of the anthers positioned in the flower centre, especially the intermediate stamens, reduced bee visits. Both results revealed a division of labour, in which the intermediate stamen morph was responsible for both floral attractiveness and pollen resources. Only the largest stamen morph produced germinable pollen grains, highlighting their role as pollinating stamens. The smallest stamen morph has a less clear function, likely representing an economy in pollen production for feeding function. Our findings suggest that the evolution of the trimorphic androecium is associated with division of labour in large pollen flowers and can represent a strong strategy for circumventing the pollen dilemma, optimizing the feeding function by reducing pollen grain investment from central anthers.

Pollen dispensing schedules in buzz-pollinated plants: experimental comparison of species with contrasting floral morphologies.

PREMISE: Plants can mitigate the fitness costs associated with pollen consumption by floral visitors by optimizing pollen release rates. In buzz-pollinated plants, bees apply vibrations to remove pollen from anthers with small pores. These poricidal anthers potentially function as mechanism staggering pollen release, but this has rarely been tested across plant species differing in anther morphology. METHODS: In Solanum Section Androceras, three pairs of buzz-pollinated species have undergone independent evolutionary shifts between large- and small-flowers, which are accompanied by replicate changes in anther morphology. We used these shifts in anther morphology to characterize the association between anther morphology and pollen dispensing schedules. We applied simulated bee-like vibrations to anthers to elicit pollen release, and compared pollen dispensing schedules across anther morphologies. We also investigated how vibration velocity affects pollen release. RESULTS: Replicate transitions in Solanum anther morphology are associated with consistent changes in pollen dispensing schedules. We found that small-flowered taxa release their pollen at higher rates than their large-flowered counterparts. Higher vibration velocities resulted in quicker pollen dispensing and more total pollen released. Finally, both the pollen dispensing rate and the amount of pollen released in the first vibration were negatively related to anther wall area, but we did not observe any association between pore size and pollen dispensing. CONCLUSIONS: Our results provide the first empirical demonstration that the pollen dispensing properties of poricidal anthers depend on both floral characteristics and bee vibration properties. Morphological modification of anthers could thus provide a mechanism to exploit different pollination environments.

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

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.

Buzz-Pollinated Crops: A Global Review and Meta-analysis of the Effects of Supplemental Bee Pollination in Tomato.

Buzz-pollinated plants require visitation from vibration producing bee species to elicit full pollen release. Several important food crops are buzz-pollinated including tomato, eggplant, kiwi, and blueberry. Although more than half of all bee species can buzz pollinate, the most commonly deployed supplemental pollinator, Apis mellifera L. (Hymenoptera: Apidae; honey bees), cannot produce vibrations to remove pollen. Here, we provide a list of buzz-pollinated food crops and discuss the extent to which they rely on pollination by vibration-producing bees. We then use the most commonly cultivated of these crops, the tomato, Solanum lycopersicum L. (Solanales: Solanaceae), as a case study to investigate the effect of different pollination treatments on aspects of fruit quality. Following a systematic review of the literature, we statistically analyzed 71 experiments from 24 studies across different geopolitical regions and conducted a meta-analysis on a subset of 21 of these experiments. Our results show that both supplemental pollination by buzz-pollinating bees and open pollination by assemblages of bees, which include buzz pollinators, significantly increase tomato fruit weight compared to a no-pollination control. In contrast, auxin treatment, artificial mechanical vibrations, or supplemental pollination by non-buzz-pollinating bees (including Apis spp.), do not significantly increase fruit weight. Finally, we compare strategies for providing bee pollination in tomato cultivation around the globe and highlight how using buzz-pollinating bees might improve tomato yield, particularly in some geographic regions. We conclude that employing native, wild buzz pollinators can deliver important economic benefits with reduced environmental risks and increased advantages for both developed and emerging economies.

Connective appendages in Huberia bradeana (Melastomataceae) affect pollen release during buzz pollination.

Floral structures, such as stamen appendages, play crucial roles in pollinator attraction, pollen release dynamics and, ultimately, the reproductive success of plants. The pollen-rewarding, bee buzz-pollinated flowers of Melastomataceae often bear conspicuous staminal appendages. Surprisingly, their functional role in the pollination process remains largely unclear. We use Huberia bradeana Bochorny & R. Goldenb. (Melastomataceae) with conspicuously elongated, twisted stamen appendages to investigate their functional role in the pollination process. We studied the effect of stamen appendages on pollinator behaviour and reproductive success by comparing manipulated flowers (appendages removed) with unmanipulated flowers. To assess bee pollinator behaviour, we measured three properties of buzzes (vibrations) produced by bees on Huberia flowers: frequency, duration and number of buzzes per flower visit. We measured male and female reproductive success by monitoring pollen release and deposition after single bee visits. Finally, we used artificial vibrations and laser vibrometry to assess how flower vibrational properties change with the removal of stamen appendages. Our results show that the absence of staminal appendages does not modify bee buzzing behaviour. Pollen release was higher in unmanipulated flowers, but stigmatic pollen loads differ only marginally between the two treatments. We also detected lower vibration amplitudes in intact flowers as compared to manipulated flowers in artificial vibration experiments. The presence of connective appendages are crucial in transmitting vibrations and assuring optimal pollen release. Therefore, we propose that the high diversity of colours, shapes and sizes of connective appendages in buzz-pollinated flowers may have evolved by selection through male fitness.