The biophysics of aerial electroreception in arthropods

We recently discovered that bumblebees can detect and learn about the electric fields that arise when they approach a flower. A weak electric field indeed builds up as bumblebees, like other flying insects, tend to be positively charged, and flowers tend to have an excess of negative charges - electrons. Using experiments that teach bee to recognize flowers with sugar rewards, it was possible to show that bee can memorise which flower contains sugar rewards on the sole basis of the flower's electric field. New evidence shows that spiders can also use electric fields; this time to fly! We could indeed show in the lab and in the field, that spiders perform ballooning flights by casting in the air several strands of their finest silk. As the spider stands on its tiptoes on top a tall grass or leaf, their silk sail experiences an uplifting force from the electrostatics in the atmosphere. Interestingly, we could show that ballooning takes also place in the total absence of wind, solving a question that Charles Darwin asked himself as he observed thousands of tiny spiders alighting the riggings of his ship, the Beagle.
Bumblebees are quite furry, a coat deemed useful to staying warm and collecting pollen. We wondered whether fine hairs can react to electric forces. We first imagined that bees may experience something similar to the hair-raising sensation we used to have when approaching an old television set. For bees and spiders, we measured the tiny hair movements as they are exposed to electric fields like those found in nature, using a fine beam of laser light. We thus discovered that bees and spiders have dedicated sensors -fine hairs- to detect weak electric fields. But do other insects detect electric fields, and why? We have chosen to study an important group of insects - beetles because they play crucial roles in global ecology and allow us to investigate other reasons why small insect may use electric fields. We have chosen ladybird larvae and dock beetles because they have distinct rows of fine hairs on their backs, the function of which is currently unknown. We hypothesise that negatively charged leaf dwelling insects use these hairs to electrically detect positively charged approaching flying predators and parasitoids, such as wasps and flies. In the field, we have observed that ladybird and dock beetle larvae react to the presence of an electric charge approaching them. We note that ladybird larvae have well-organized rows of hair tufts, the function of which is unknown. Here, we seek to establish whether the detection of electric field also pertains to predator or prey detection, functions that go beyond that of pollination and that is relevant to many insect species that play important roles in ecosystems and agriculture.

Weak electric fields are pervasive in the natural environment, but apparently, are not sensed by humans. Our work also aims at increasing our awareness, shaping a better understanding of the electric environment, our electric ecology. Our research project therefore serves to developing new ways to measure and understand the existence of this potentially important component of the sensory ecology of humans, animals and plants. We will be collecting data and producing visual media that will make visible this thus far elusive part of the natural world. We will employ our novel electrical measurement and visualisation techniques, learning from the way small insects detect weak electric fields. Using 3D printing techniques, we will model, design and construct insect-like hair structures made of electrically chargeable plastics. This bio-inspired approach will contribute to the long-term impacts of this research. As such, our research will also provide scientific information enabling more general questions about the possible impacts of man-made electric fields on humans, the environment and the organisms supporting important ecological networks and services.

This research will empirically and mathematically investigate the sense of aerial electroreception (AE) in insects. We will investigate AE in beetles, a speciose group of animals that plays important roles in ecological networks. Research will expand our understanding of the ecological functions and mechanisms of AE in terrestrial arthropods, offering a novel class of explanations for morphologies, behavioural adaptations and evolutionary radiations in arthropods. This proposal exploits our discoveries of AE and hair-based mechanisms of detection in bumblebees. The electromechanical sensitivity of fine hairs was found to exceed their acoustic sensitivity, a strong indication of the presence of an adaptive mechanism for electromechanical coupling between bees and floral electric fields. Yet, large gaps remain in our understanding of AE, its functions and the diverse mechanisms supporting this sensory modality. We chose to focus on ladybird larvae and dock beetles as they are respectively predators and herbivores that live in contact with leaves, typically negatively charged waxy surfaces. They also are prey to aerial predators, such as wasps, which are positively charged. This charge separation generates a Coulomb force, like that arising between bees and flowers. Using picoammeters and picoelectrometers, we will characterise the electric fields surrounding these insects placed on plants. The electromechanical sensitivity of dorsal hairs will be characterised using microscanning laser Doppler vibrometry and Kelvin probe force microscopy. Field and lab tests will establish behavioural sensitivity and repertoire to electric fields mimicking approaching predators. A formal mathematical analysis will provide predictive modelling that will help formalise mechanisms, length scales and topologies of the multiscale problem of AE. Beyond bee flower interactions, we will test the hypothesis that AE can be used in prey and predator detection, mate finding and navigation.

The outcomes of the planned research will foremost benefit researchers in the field of sensory biology. We know from our regular contributions to scientific meetings in atmospheric physics, meteorology and the EU network ELECTRONET, that several other disciplines related to the studies of atmospheric physics, chemistry and human health are interested by both our empirical and theoretical approaches and research goals and hypotheses. For example, our ongoing development of quantitative, reliable and very sensitive instrumentation enabling small scale measurements of electric fields has attracted the attention of academic beneficiaries and environmental monitoring agencies. Scientists in the fields of physics, chemistry and biology have expressed their interest in our findings. Here, our past and planned studies on the sensitivity of organisms (bees, spiders, beetles and other arthropods) to local electrostatic charges and electric potentials opens the door to further revealing the ubiquity and pervasiveness of a novel sensory modality. For biologists and scientists alike, the opportunity is rare to be able to discover, explore, exploit and share the discovery of a new sense. The use of electric fields as a source of ecologically relevant information by small animals provides an entirely new vista and explanations on how and why organisms organise their lives in time and space - the essence of ecological research.

Specifically, because many insect species provide key ecological services and herbivorous insects constitute constant threats to crops, we expect impact to also reach researchers and policy-maker in the areas of research in the sustainability of ecosystem supporting food production.

With a more general view, it is fair to say that in the past hundred years, the world has become electrical. Our environment now harbors a vast network of electric wires and antennae, generating electric fields and electromagnetic waves constantly percolating through our living habitats. Our research is expected to impact on our fundamental understanding of what we see as our electric ecology, by analogy to visual or auditory ecologies. We still know very little about electric ecology, as part of the natural or anthropic world. Our research has direct impact on how scientists will further understand ecosystems and key species -pollinators and herbivores- that are underpinning food webs and globally impact on important ecological and agricultural systems. Hence, our work has also direct relevance to national and global food security.

The outcomes of the research planned will also appeal to a broad cross-section of the public as part of an increasing awareness of the beauty and complexity of the natural world. Our findings will highlight and inform individual and societal responsibilities to monitor and guarantee sustainability of this natural world. As detailed in our Pathways to Impact document, we will directly engage with the media, science festivals, environmental charities and other organisations. The public will thus actively benefit from our activities through the electronic media (web pages, twitter, YouTube channel), but also through activities at science festivals, contributions to the general press, and television and radio interviews.

In conducting this programme of research, the team assembled in the PI and Co-I's labs will gain further training and experience in project and personnel management, as well as developing strong communication skills through public engagement and industry and policy-driven knowledge exchange activities. Importantly, we will ensure that training is delivered to our entire team, and that of volunteers, enhancing the educational value of impact, and generating increased opportunities for science to engage with the public and policy makers, teachers, school children, industrial partners and fellow academic researchers.