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.

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 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.

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.

How and why do bees buzz? Implications for buzz pollination

Buzz pollination encompasses the evolutionary convergence of specialised 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 categorised according to their mode of production and deployment into: (1) thermogenic, which generate heat with little mechanical vibration; (2) flight buzzes, which combined with wing deployment and thoracic vibration, power flight, and (3) non-flight buzzes in which the thorax vibrates but the wings remain folded, and include floral, defence, mating, communication, and nest-building buzzes. I hypothesise 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 optimise energy use and pollen collection.

Role of Bumblebees (Hymenoptera: Apidae) in Pollination of High Land Ecosystems: A Review

Bumblebees are one among the anthophilous form and play a significant role in the pollination of major agricultural crops like medicinal, aromatic, ornamental and various other horticultural plants. They are abundant and mostly confined to flowers present in the temperate, alpine and arctic climates of the northern continents. The bumblebees are considered as most important pollinators and are mainly responsible for the conservation of high altitude vegetation germplasm where other insect pollinators are very much limited. They are more successful pollinators and can visit large number of flowers per minute than other bees and are perfect for picking up and transferring appreciable amount of compatible pollen to flowers and thus perform buzz pollination. It is quite evident that the population of bumblebee is gradually declining throughout the globe for the last 7 decades due to agricultural intensification, habitat loss, deforestation, overgrazing, pesticide poisoning and climate change. The present paper addresses this issue on the basis of literature survey.

Are flowers tuned to buzzing pollinators? Variation in the natural frequency of stamens with different morphologies and its relationship to bee vibrations

During buzz pollination, bees use vibrations to remove pollen from flowers. Vibrations at the natural frequency of pollen-carrying stamens are amplified through resonance, resulting in higher-amplitude vibrations. Because pollen release depends on vibration amplitude, bees could increase pollen removal by vibrating at the natural frequency of stamens. Yet, few studies have characterized the natural frequencies of stamens and compared them to frequencies of buzz-pollinating bees. Here we use laser Doppler vibrometry to characterise natural frequencies of stamens of six buzz-pollinated Solanum taxa of contrasting stamen morphology. We also compare the fundamental frequency of bumblebee buzzes produced on two Solanum species with different natural frequencies. We found that stamen morphology and plant identity explain variation in natural frequency of stamens. Our results show that medium-sized pollinators, such as bumblebees, produce buzzes of frequencies higher than the natural frequency of most (5/6) of the Solanum species we studied. However, the observed natural frequency of Solanum stamens is at the low end of the range of frequencies produced by other buzz-pollinating bees. Thus, our findings suggest that in some buzz pollination interactions, but not others, stamen resonance may play a role in mediating pollen release.