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Mechanisms of electroreception in bees and other terrestrial animals

Periodic Reporting for period 4 - ElectroBee (Mechanisms of electroreception in bees and other terrestrial animals)

Período documentado: 2022-03-01 hasta 2024-02-29

The project was aiming at generating transformative information on the sense of electroreception in air in terrestrial arthropods. For context, work served to identify the how and why of electroreception in bees and other arthropods, characterizing the the potential diversity in structures and functions that enable aerial electroreception. The project unveiled the diversity of this recently discovered sensory modality, in a broad context of interactions between animals, plants, and atmospheric electricity. In effect, beyond bees, the project has investigated aerial electroreception in other arthropod species, namely caterpillars from several moths and butterfly species, treehoppers, ticks and spiders. The generality of aerial electroreception has thus been addressed, with particular attention to behavioral and morphological adaptations, but also with respect to mechanisms of detection. Complementarily, theoretical work has been produced to explore the possibilities, and physical properties of aerial electroreception, considering both physical and biological sources of information.

A salient outcome resides in the fact that aerial electroreception is proposed to be a new sense, equivalent in adaptive value to vision, olfaction or hearing. We propose that it is present in many arthropod species, a proposition that has never been considered before. Our work has established that electroreception is possible outside the aquatic environment, where it has been scientifically studied for some 65 years. All objectives have been reached, as we have gathered empirical evidence supporting our original hypothesis and have developed a general theoretical framework that demonstrates biological and physical realizations and capabilities of aerial electroreception with multiphysical and mathematical models.

The outcomes of the ElectroBee project are likely to contribute to evaluating whether the electric ecology of natural environments is affected by human activity. With humans, the world has become very electrical. The presence of anthropogenic electric fields, magnetic fields, and electromagnetic fields in the environment is very novel in evolutionary terms. What we have shown is that electrostatics and electroreception is an old sense that predates the deployment of electricity by humans. This may have consequences for wildlife and humans alike, much like light and acoustic pollutions are increasingly recognized for their effects on natural systems and organisms. Global electrification generates alterations in the physical and sensory ecologies of organisms. Studying an evolved sense, as we have done, and characterising it in its natural condition can help appreciate the natural baseline, the state against which recent changes and potential disruptions for the health of ecosystems and their organisms can be measured. Using our theoretical framework we may be in a good position to evaluate rapidly changing situations, predict outcomes and future trajectories, assess environmental health, and consider realms of applications of mitigations and evidence-based norms of emissions. As such, studying electroreception in air, whilst uncovering an entire sensory world previously unknown, offers the possibility to develop analytical tools to measure anthropogenic effects on wildlife and humans.
The breakthrough arising from ElectroBee resides in establishing that Aerial Electroreception is a novel sensory modality. For example, the fact that some organisms are always electrostatically charged, and some others seek not to be revealed entirely new detection and cryptic strategies used for survival. Overall, our research has shown that, electroreception in terrestrial arthropod can be a sufficient and sometimes necessary sense useful in their ecology. This is in fact like other senses, but with vastly different physics and sensory mechanisms, and behaviours. More directly, this previously unknown sense has now been revealed through our research. We have also many reasons, that are explained at length and in details in multiple publications, to propose that this sense is very widespread among terrestrial arthropods. Our work has opened up a large field of sensory biology, and possibly another way to “see” the world around us. Altogether this comes in support of my original general hypothesis stating that “aerial electroreception is a diverse and widespread sensory modality across arthropod species”.

We have completed work on all work packages. WPs related to instrumentation development has yielded valuable outcomes, generating bespoke instrumentation and one in particular is the microFaraday pail that pushes the capabilities of such instruments (Harrison & Robert 2025, J, Electrostatics). For example, we have been able to break a length scale barrier with a new laser Doppler vibrometer, allowing us to measure electromechanical actuation with unprecedented spatial accuracy. Using our state of the art low-noise labs at the University of Bristol (Robert lab), the resolution obtained in the magnitude of vibration is ground-breaking, in the picometer range. To facilitate perspective, it might be noted that 10 pico metres are to a metre what the stone of a cherry is to the earth. Such resolution allows us to establish that very weak electric fields have an electromechanical effect on selected cuticular structures. The putative sensors are being now identified. Another progress is the development of techniques to "make electric visible". How do we know about the existence of electric field arising between a flower and a pollinator such as a bee? How do we know about the field between an insect sitting on the surface of a leaf, the leaf, and the predatory wasp searching for its prey? These questions necessitate the characterisation of electric fields, in magnitude, dynamics and structure. For this objective we have dual electrometers and pico ammeters that report on electric field and electric induction respectively at the length scale required by leaves and insects, in the order of 5-10 cm. We have also made progress on plant, establishing that there is electro-activity of plants within an atmospheric electric gradient that acts by inductive interaction.
The results with the new laser technology is beyond state of the art. In general, as mesoscale electric field imaging is not very well developed in physics, there is ample space for further instrumentation development. Mindful of the limitation in scope and length of this project, we consider our activities as innovative with this respect. With expert colleagues in the UK, we have developed an ultra sensitive mesoscale Faraday cup that pushes current limits. We have generated two review and integrative publications with EU colleagues that contribute to set up the large scope of the roles of electrostatics, atmospheric electricity and bio-meteorology. We communicate our progress to colleagues in the atmospheric physics and biometeorology communities. More specifically, we expect to contribute broadly and specifically to deeper appreciation of the role of weak electric fields and triboelectrification in animals, plants and their possible role in adapted behavioural strategies in the course of biological evolution. As sated above, we anticipate our activities to have an impact on our understanding of the effects of anthropogenic "industrial and post-industrial electrification".
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