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Mechanisms of electroreception in bees and other terrestrial animals

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Electroreception in air: invisible strands of connection all around us

Research has shown for the first time that bumblebees not only sense the tiny voltage given off by flowers but can use weak electric fields to identify which flowers have already been visited by other bees.

Electroreception, the ability to detect electric fields in an environment, has mainly been studied in aquatic vertebrates: sharks and rays, electric fish and, intriguingly, the platypus. Water acts as the conductive medium. But electricity is in the air around us: the hairs on our arms rise when we are around a cathode ray. This is an example of electroreception in a non-conductive medium, or ‘aerial electroreception’ (AE). Pollinators and the plants they are attracted to are dependent on one another. What role does AE have in such tightly symbiotic relationships? “For bees and spiders, sensing electric fields is literally a hair-raising experience. We can show that an electric field, such as that present between a bee and a flower, can deflect the little hairs they have on their head and their legs,” says Daniel Robert, professor of Bionanoscience at the School of Biological Sciences, part of the University of Bristol. The ElectroBee project, which received funding from the European Research Council, was borne out of the realisation that a new sensory modality, to which we humans are insensitive, a hidden sensory dimension, was playing out without us knowing.

Laser Doppler vibrometer measuring reactions down to the nanometre

The research is delving into a world filled with tiny signals and receptors, so Robert and his team harnessed the power of laser Doppler vibrometry to measure the motion of hairs at the scale of a nanometre. As he explains: “To give an impression of the scale, a nanometre is to a metre, what an apple is to the Earth. Such small motions can be detected by the sensitive neurones at the base of many hairs on insects.” To assess whether bumblebees could sense electric signals, ElectroBee took a bumblebee colony and allowed them to fly in an arena in the laboratory, where conditions could be measured and controlled. The bees were offered two types of feeding stations, which provided either sugar water, which they seek, or quinine, which they do not like. All feeding stations looked identical, but the feeding stations were also designed to be electric platforms, or e-flowers. “We were able to control the voltage and we set the sugar water-providing feeder at 30 volts, a small voltage mimicking an average flower potential, and set the quinine feeders at zero volts.” The feeders were moved after each visit to prevent bumblebees from learning the position of feeders and the overall geometry of the arena. “We found that the bees can learn to find the source of sugar, associating the electric field with it. Tellingly, when we switch all e-flowers off, and repeat the process, the bees were unable to learn where the sugar water was.”

Getting bees to fly through hoops

But to accurately tune the level of voltage bees experience from flowers, the team also had to be sure they were using a relevant level of electrostatic charging. This is where copper hoops came into play. “We could measure these amounts by letting the bumblebees fly through a ring made of copper that is then connected to a highly sensitive instrument measuring current,” adds Robert. Knowing how much charge is present in natural interactions, the team could then recreate it by rubbing a nylon ball on a piece of plastic in just the right way, using a bit of practice, and then presenting it to the bumblebee under the laser light. “Rather like rubbing a balloon at a birthday party and watching a kid’s hair stand on end,” notes Robert.

An invisible tapestry of interaction

Mammals all have hairs made of keratin which are good at accumulating charge, so there is a possibility AE could be widespread. But what is the benefit? “When a flower has been visited, its visual appearance does not change. It has the same colour, the same shape, the same smell. But its electric potential has changed, a change that is quick and that betrays the visitation that just took place by a previous bee. The advantage is that the recent history of that flower can be read in its electric status,” explains Robert. It’s not just bees. AE helps spiders to perform ballooning behaviour which enables them to fly over distances of hundreds of kilometres. For caterpillars, it enables then to detect their electrically charged wasp predators as they approach. ”We have now been able to document multiple examples of AE with adaptive value and there are certainly many more awaiting scientific attention.” The research is significant, and has been written up in several scientific journals, because it is the first to demonstrate that electric fields transmitting through the air can be detected and learned by bumblebees, and other terrestrial arthropods. “As we got better at measuring tiny electric fields on bees, spiders, flowers and caterpillars I started to see in my ‘mind’s eye’ what the electrostatic world may look like: flowers on a meadow lighting up when bees fly past. Or spider silk projecting straight up in the sky, like laser lights, pulling them into a long voyage,” says Robert. “Evocatively, I see these electrostatic forces as fleeting, tiny strands of electricity being constantly made and unmade: connections between organisms that evoke the complexities of the fabric of life.”

Keywords

ElectroBee, European Research Council, bees, aerial electroreception, voltage, electrostatic forces, adaptive value, flowers, pollinator

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