A buff-tailed bumblebee approaches a flower of the buzz-pollinated buffalo bur. © Vallejo-Marín.

By Mario Vallejo-Marin

It is often said that bumblebees should not be able to fly. Their heavy bodies and relatively small wings provided an early challenge to aeronautic buffs in explaining how these furry insects were able to take off, let alone manoeuvre in the air while searching for food among flowers. Yet, bumblebees are accomplished flyers, and their success in the air is in part due to strong thoracic muscles that allow them to beat their wings faster than a neuron can fire. But these flight muscles are also responsible for a little known trick that only bees can do: they can pollinate flowers using high frequency vibrations.

Bees are avid pollen-eaters that depend on pollen grains as a source of protein for the development of their larvae. A single bee can collect millions of pollen grains in a single day. In exchange for the pollen provided to these hungry pollinators, plants gain the match-making services of a highly mobile insect, ensuring that fertilisation between flowers occurs. Yet, the price paid by plants in pollen currency can be overwhelming.

In the many plant species that have lost the capacity to produce nectar—the sugary “treat” offered to animals visiting flowers—pollen takes on two contrasting jobs: it is the carrier of sperm cells needed for fertilising ovules, and simultaneously becomes the main reward to attract pollinators. Thus a plant has to do a difficult balancing act providing pollen to visiting insects, but ensuring that pollinators do not consume it all in one go. As fertilisation is a game against the odds (only about one pollen grain in a thousand will successfully reach another flower), flowers benefit from distributing their pollen load in as many pollinators as possible. In contrast, pollen-consuming insects want to collect as much pollen as energetically viable.

The evolutionary solution of more than 15,000 species of flowering plants to the efforts of pollen-consuming bees has been to make access to pollen grains in flowers trickier. In these plant species, the pollen is not freely available, but instead is protected within male reproductive organs, anthers, that only release pollen from tiny pores. Imagine a salt shaker with tiny orifices. Bees have figured out the most efficient way to extract the protein-rich pollen grains from these “poricidal” anthers: they use their powerful flight muscles to produce high frequency vibrations that cause the pollen grains to bounce inside the anthers, acquiring enough energy to eventually catapult the pollen out of the anther like a miniature geyser and onto the bee’s body. The vibrations produced by the bees while extracting pollen are so powerful that they have to hold on to the anthers with their mandibles, otherwise they would probably be thrown off the flower.

Buzz-pollination, as this phenomenon is known, is a widespread mode of reproduction in thousands of plant species, including many agriculturally important species such as tomatoes, potatoes, aubergine, and even kiwi fruit. Without buzz-pollination, many of plant species struggle to reproduce at all. Yet our knowledge of this fascinating phenomenon is still in its infancy.

The relationship between “buzz-pollinated” flowers and their vibrating insect visitors has caused some amazing macroevolutionary patterns. For example, buzz-pollinated species among disparate plant families have converged to similar flower morphologies (the “tomato” flower). However, it is virtually unknown if plant species with varied morphologies require different types of vibrations to release pollen. From a bee’s perspective, not all vibrations produced are necessarily equal. Although bees also produce vibrations when threatened (buzzing-off predators), these defensive buzzes have different characteristics from those produced during pollen collection. Moreover, it has recently been shown that different species of bumblebees produce different types of vibrations (at different frequencies) when visiting the same flower. Yet, the effect of species-specific “tuning” on pollen removal is little understood. Even more basically, it is not known why some bees are expert buzz-pollinators, for example bumblebees, while others seem incapable of it, such as honeybees, even when both seem to have the required muscle machinery.

Much remains to be learned about the use of vibrations to pollinate flowers. Some of these questions relate to basic issues in biology such as coevolution between plants and pollinators, natural selection, behavioural ecology, and the association between form and function in biological structures. Other aspects of buzz-pollination could have important applied consequences. For example, if bees vibrate at different pitches, are certain species of bees better suited to pollinate specific crops? Could we improve crop pollination by supplementing agricultural fields with particularly “good” buzz-pollinators for a given type of plant? At the very least, the study of buzz-pollination reminds us of the beautiful and delicate evolutionary balance between plants and their pollen-eating visitors. The ability of some, but not all, bees to obtain their food through vibrations is a powerful reason to strive towards conserving the widest range of bee species possible, as saving one bee group may not be enough. Thousands of plant species depend on these “food vibrations” to reproduce.

Mario Vallejo-Marín

www.plant-evolution.org

You can find out more about buzz-pollination here: http://www.plant-evolution.org/wp/in-the-news/

If you are interested in studying buzz-pollination at Stirling either as a graduate career or as a summer volunteer on one of our research projects, please drop me a line: mv9@stir.ac.uk