Structural Dynamics of Real and Modeled 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 large vibratory forces to the flower stamen by rapidly contracting its flight muscles. The resulting deformation and pollen expulsion depend critically on the stamen's natural frequencies and vibration mode shapes, yet these properties remain unknown. 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.

PLoS Computational Biology Issue Image | Vol. 17(9) October 2021

The tomato flowers are characterized by possessing poricidal anthers, which restrict the exit of the pollen to a tiny opening on the apex of the anther. To extract pollen efficiently, some visiting bees grasp the anthers and quickly contracting their flight muscles, producing vibrations and an audible sound. The vibrations are transferred to the anthers, shaking and stimulating the pollen inside them to leave by the pores, a phenomenon known as floral sonication or buzz-pollination. DOI: pcbi.1009426 Image Credit: Priscila de CE1;ssia Souza AraFA;jo (co-author of the manuscript) photographed this bee visiting flowers of tomato plants grown at the experimental fields of the Federal University of ViE7;osa (Minas Gerais State, Brazil). We confirm that the image can publish under the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/). The authors own the copyright for the image and confirm that agree with open Access License of PLOS Computational Biology.

PLoS Computational Biology Issue Image | Vol. 1(9) October 2021

The tomato flowers are characterized by possessing poricidal anthers, which restrict the exit of the pollen to a tiny opening on the apex of the anther. To extract pollen efficiently, some visiting bees grasp the anthers and quickly contracting their flight muscles, producing vibrations and an audible sound. The vibrations are transferred to the anthers, shaking and stimulating the pollen inside them to leave by the pores, a phenomenon known as floral sonication or buzz-pollination. DOI: pcbi.1009426 Image Credit: Priscila Souza AraFA;jo (co-author of the manuscript) photographed this bee visiting flowers of tomato plants grown at the experimental fields of the Federal University of ViE7;osa (Minas Gerais State, Brazil). We confirm that the image can publish under the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/). The authors own the copyright for the image and confirm that agree with open Access License of PLOS Computational Biology.

Reduced visitation to the buzz-pollinated Cyanella hyacinthoides in the presence of other pollen sources in the hyperdiverse Cape Floristic Region

Many plant species have floral morphologies that restrict access to floral resources, such as pollen or nectar, and only a subset of floral visitors can perform the complex handling behaviours required to extract restricted resources. Due to the time and energy required to extract resources from morphologically complex flowers, these plant species potentially compete for pollinators with co-flowering plants that have more easily accessible resources. A widespread floral mechanism restricting access to pollen is the presence of tubular anthers that open through small pores or slits (poricidal anthers). Some bees have evolved the capacity to remove pollen from poricidal anthers using vibrations, giving rise to the phenomenon of buzz-pollination. These bee vibrations that are produced for pollen extraction are presumably energetically costly, and to date, few studies have investigated whether buzz-pollinated flowers may be at a disadvantage when competing for pollinators' attention with plant species that present unrestricted pollen resources. Here, we studied Cyanella hyacinthoides (Tecophilaeaceae), a geophyte with poricidal anthers in the hyperdiverse Cape Floristic Region of South Africa, to assess how the composition and relative abundance of flowers with easily accessible pollen affect bee visitation to a buzz-pollinated plant. We found that the number of pollinator species was not influenced by community composition. However, visitation rates to C. hyacinthoides were negatively related to the abundance of flowers with more accessible resources. Visitation rates were strongly associated with petal colour, showing that flower colour is important in mediating these interactions. We conclude that buzz-pollinated plants might be at a competitive disadvantage when many easily accessible pollen sources are available, particularly when competitor species share its floral signals.

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

In buzz-pollinated plants, bees apply vibrations to remove pollen from anthers that have small apical pores or slits. These poricidal anthers potentially function as mechanism to stagger pollen release, but this has rarely been tested across plant species differing in anther morphology.In Solanum section Androceras, three pairs of buzz-pollinated Solanum species have undergone independent evolutionary shifts between large- and small-flowered taxa. These shifts in flower size are accompanied by replicate changes in anther morphology, and we used these shifts in anther morphology to characterise the association between anther morphology and pollen dispensing schedules. We characterised pollen dispensing schedules by applying simulated bee-like vibrations directly to anthers to elicit pollen release. We then compared pollen dispensing schedules across anther morphologies, and we further investigated how vibration velocity affects pollen release. Finally, we assessed whether particular anther traits, presented in the Buchmann-Hurley model, can predict pollen dispensing schedules.We show that replicate transitions in Solanum anther morphology are associated with consistent changes in pollen dispensing schedules. We found that small-flowered taxa with small anthers release their pollen at higher rates than their large-flowered counterparts, showing an association between general anther morphology and pollen dispensing. Further, higher vibration velocities resulted in quicker pollen dispensing and more total pollen released, which suggested that bees that produce high-energy vibrations can access more reward than bees producing low-energy vibrations. Finally, both the pollen dispensing rate and the amount of pollen released in the first vibration were negatively related to anther wall area, but, surprisingly, we did not observe any association between pore size and pollen dispensing.Our results provide the first empirical demonstration that the pollen dispensing properties of poricidal anthers depend on both floral characteristics and bee vibration properties, and suggest that morphological modification of anthers could provide a mechanism to exploit different pollination environments.

Low endemic bee diversity and very wide host range in lowland Fiji: support for the pollinator super-generalist hypothesis in island biogeography

The success of invading plants in island ecosystems has often been inferred to result from ‘invader complexes’, where cointroduced plants and their specialist pollinators can reciprocally enhance each other’s spread. However, it has also been suggested that in islands with low pollinator diversity, those pollinators should evolve into super-generalists that may be able to pollinate a wide range of exotic plants, enabling the spread of exotic weeds. Fiji has a very depauperate endemic bee fauna and previous studies have suggested that its only lowland bee species, Homalictus fijiensis (Apoidea: Halictidae), has a very wide range of host plants. However, those studies only included a small number of endemic flowering plants. Our study expands observations of bee–flower interactions to explore host plant ranges of H. fijiensis and introduced bee species to include a wider variety of native and introduced plant species. We show that H. fijiensis does have a wider host range than introduced bees, including Apis mellifera (Apoidea: Apidae), and an ability to exploit extrafloral nectaries and poricidal anthers that are not utilised by the introduced bee species. Our results support the hypothesis that super-generalism can evolve in islands where pollinator diversity is low, and that this may make those islands susceptible to weed invasions.

A new species of Ochna (Ochnaceae) from the Barberton Mountains of Mpumalanga, South Africa

Ochna barbertonensis is described as a new species from the Barberton Mountains in Mpumalanga, South Africa. The new species is characterised by its suffrutescent habit, elongate-deltoid stipules sometimes with broadened base, mucronate leaf tip and high anther to filament ratio, where the anthers are ca. two times longer than the filaments. It is placed within sect. Ochna due to its poricidal anthers and subglobose drupes, attached at the base. It is most likely to be confused with the superficially similar suffrutescent species Ochna confusa, but that species has longitudinal anther dehiscence and anthers shorter than the filaments. The new species occurs within well protected nature reserves, but is only known from five collections with an Extent of Occurrence (EOO) of 34 km2, making it a ‘Rare’ species under the Red List of South African Plants. A species description, illustration and distribution map are provided.

Reproductive biology of endemic Solanum melissarum Bohs (Solanaceae) and updating of its current geographic distribution as the basis for its conservation in the Brazilian Cerrado

The genus Solanum (family Solanaceae) includes more than 1400 species and has buzz-pollinated flowers with poricidal anthers. The present study aimed to describe the distribution, breeding system and pollination mechanism of Solanum melissarum, a species endemic to Brazil. The study of breeding system was conducted in an urban forest fragment in Jataí, GO. Distribution data were gathered from floristic surveys and digital plant databases. The floral morphology and the pollination mechanism were studied on through field observations and preserved flowers. The breeding system was determined through hand pollination treatments. The species has a distribution only in the Brazilian Atlantic forest coastal, and this study provides the first records of S. melissarum for the state of Goiás. The pendulous flowers have poricidal anthers close to the stigma, with membranous thecae joined by a connective bearing osmophores that attract males of Euglossa cordata bees. As they collect fragrances, the bees press the thecae and pollen is released through a bellows mechanism. Based on the hand-pollination treatments, this species is self-incompatible. Isolated forest fragments may not include enough pollinators to ensure the pollination of plants with specialized systems. However, they are essential for the conservation of species with interesting phytogeographic patterns, such as the vicariance observed in S. melissarum, and for the conservation of regional diversity.