The mechanisms of electroreception in bees

Lead Research Organisation: University of Bristol
Department Name: Biological Sciences

Abstract

The ecological partnership between flowers and bees is profound; flowers evolved spectacular displays of colours and fragrant volatiles to attract pollinators, in particular bees, to secure pollen transfer and fertilisation. Many flowers include nutritious nectar as a special reward. Both bee and flower benefit from this remarkable example of cooperation. Thus, bees can see and smell flowers, but is that all? Our research changed its path when we marveled at the fact that a flower's pollen is capable of jumping towards an approaching bee and sticking to it. Driven by electrostatic forces, the pollen is transported from flower to flower. But is this the only way electricity can enhance pollination? Following these observations, a simple question came to our minds: does the bee know anything about the presence of this electrostatic field?

Recently, we reported that bumblebees (Bombus terrestris) can detect and learn about floral electric fields. These fields are in fact floral cues, complementing colour, scent, temperature, humidity and shape. Floral fields are affected by the visit of bees, which are also electrically charged. Like visual cues, floral electric fields exhibit variations in pattern and structure, which can be discriminated by bumblebees. We also showed that electric field information can improve a pollinator's memory of floral rewards. Because floral electric fields can change within seconds, their detection may facilitate rapid communication between flowers and their pollinators. Yet, how bees detect floral electric fields remains unknown.

The goal of the proposed research is to identify the sensory mechanisms by which a bee detects electric fields. Do bees have a dedicated electric sensory organ, like many animals have dedicated ears to detect sounds? We hypothesise that bees use the fine hairs on their bodies to sense the presence of floral electrostatic fields. This is similar to the sensation we experience from the hairs on our arm rising in front of an old television set. We will measure the deflection of bee hair and record the activity of sensory neurones at their base. We will also train bees to recognise different electric fields and, after impairing the bending of these hairs, evaluate their recognition ability. Using mathematical modelling and laser vibration technology, we will also establish the kind of electric fields that bees are in effect sensitive to. Are they only sensitive to floral fields?

This work will describe an entirely novel sense. The role this electrical sense plays in the life of bees including their mutualism with flowers, is still poorly understood. Do other important pollinators, such as flies, beetles and moths also sense floral electric fields?

Our work will also change the way we understand our environment and its complexity, adding an electric component. Currently we are blind to this electrical ecology; yet this research project aims at providing ways to visualise this thus far elusive part of the natural world. Potentially, novel electrical measurement techniques, perhaps bio-inspired, will emerge from our investigations on detection of weak and local electric fields. As such, the interest of technologists may also be important to the long term continuation and diversification of our research and its impacts.

Also, our research will enable further questions to be asked about the possible negative or positive, but currently unknown, impacts of man-made electric fields on pollinators, and other organisms, including plants, and the environment. As bees provide important and valuable pollination services for many crops consumed by humans, it may be very timely to better understand the biology of bees, and ensure they can remain safe and healthy in a rapidly changing and uncertain environment.

Technical Summary

We recently discovered that bumblebees (Bombus terrestris) can detect and learn about floral electric fields. Our discovery establishes the existence of a formerly unknown sensory modality in terrestrial animals. Bees use several senses to detect flowers, sensing floral cues such as colors, shapes, patterns, fragrant volatiles and humidity. Weak electric fields can also act as floral cues. Like visual cues, floral electric fields exhibit variations in pattern, which bees can discriminate. We established that such electric field information improves the bee's memory of floral rewards. Bees can remember to associate food rewards with a particular electric field. This is evidence of a well-developed sensory system.
Our central objective is to establish how bees detect floral electrical fields.
The goal of the proposed research is to identify the sensory mechanisms by which bee detect electric fields. We will establish whether bees have dedicated electric sensory organs. We hypothesise that bees use the fine hairs on their body to sense electrostatic fields. We know that such hair can be deflected by incident weak electric fields. To test this hypothesis, we will measure the mechanical deflection of bee hair and record the activity of sensory neurones at their base. We will extend this test to the bee's antennae. We will train bees to recognise different electric fields and, after impairing hairs motion (or antennae), evaluate their recognition ability. Using mathematical modeling, we will establish the electric parameter space that bees are sensitive to in nature.
The planned work will change our appreciation of the environment by adding an electric component. Humans are apparently not sensitive to an electrical ecology, only visible to bees. Our research aims at providing novel ways to visualise and understand this elusive part of the natural world, where man-made electric fields may impact positively or negatively on the life of pollinators and other organisms.

Planned Impact

The planned research will benefit those in the field of sensory biology. Several other disciplines related to the studies of atmospheric physics and chemistry will be interested by our approach and research rationale aimed at both large and small scale measurements. Scientists in the fields of physics, chemistry and biology are interested, and more specifically those working on atmospheric physics, methods for local weather predictions. Because bees provide extremely important ecological services, we expect impact to also reach researchers and policy-maker in the areas of research in the sustainability of food production.

Our discovery of a new sensory modality, through its first reporting in the journal Science, has generated broad interest in the scientific community. Through the emails we received we know that the curiosity of a wide range of scientists of all trades, from astrophysics, atmosphere and climate scientists, and weather forecasters.

In the past hundred years, the world has become electrical, with a vast network of wires, and more recently electromagnetic waves constantly percolating through our living habitats. Our research is expected to impact on our fundamental understanding of electric ecology, a part of the natural world we know very little about. This research has direct impact on how scientists will understand ecosystems and key species -pollinators- that are underpinning food webs and providing globally important ecosystem services. Our work has 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 festival, 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 in science festivals, contributions to the general press, and television and radio interviews.

In conducting this programme of research, the team (especially the PDRAs) 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.

Publications

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Clarke D (2017) The bee, the flower, and the electric field: electric ecology and aerial electroreception. in Journal of comparative physiology. A, Neuroethology, sensory, neural, and behavioral physiology

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Matthews J (2019) Urban and rural measurements of atmospheric potential gradient in Journal of Electrostatics

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Morley EL (2018) Electric Fields Elicit Ballooning in Spiders. in Current biology : CB

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Nicoll K (2019) A global atmospheric electricity monitoring network for climate and geophysical research in Journal of Atmospheric and Solar-Terrestrial Physics

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Sutton GP (2016) Mechanosensory hairs in bumblebees (Bombus terrestris) detect weak electric fields. in Proceedings of the National Academy of Sciences of the United States of America

 
Description One of the objectives of the research is to establish the sensory basis for electroreception in bees.This is great news. What we have discovered that the fine hairs borne on a bumble bee deflect in the presence of an electric field. We find that the strength of electric field (in Volts per meter) that deflect the hairs can be very small, such as that surrounding a flower in nature. We also find that when the hair reflects, the mechanically sensitive neurone located at its base singles this event. The hairs are thus potentially part of an electromechanical detection system.

Also, in the course of the research, we have discovered that the biophysics of electroreception in air can more diverse than previously surmised. Whilst continuing on hair-based detection, we are also searching for different possible mechanisms. Behavioural and electrical evidence shows that alternative mechanisms may be at work, in parallel, and non-exclusively with the hair-based system.One of the objectives of the research is to establish the sensory basis for electroreception in bees.This is great news. What we have discovered that the fine hairs borne on a bumble bee deflect in the presence of an electric field. We find that the strength of electric field (in Volts per meter) that deflect the hairs can be very small, such as that surrounding a flower in nature. We also find that when the hair reflects, the mechanically sensitive neurone located at its base singles this event. The hairs are thus potentially part of an electromechanical detection system.

So, in the course of the research, we have discovered that the biophysics of electroreception in air can more diverse than previously surmised. Whilst continuing on hair-based detection, we are also hunting for different possible mechanisms. We have been able in the past year, to extend our search for other putative detectors of aerial electric fields. We have now a series of candidates that we are testing, in other insects mainly. In bees, we have identified a potential new form of receptor, not based on hair mechanics, but on a capacitive sensor. This is the subject of a large publication still in preparation - with hopefully a large impact. A discovery that came late in the course of this research, and serendipitously so, is the study of electrically powered flight by spiders. This had a large press impact, and enhanced general knowledge about atmospheric electricity and its effects on biological organisms and perhaps beyond this, on the organisation of aerial dispersal in migrating species.
Exploitation Route We have published additional papers and deposited data on line.

We have

It is too early to talk about technology transfer, but contacts and new collaborations have developed that may offer opportunities for particular technological outcomes.
Sectors Agriculture, Food and Drink,Education,Electronics,Energy,Environment,Healthcare,Transport

URL https://youtu.be/fZqcuUZiz6Q
 
Description The findings so far have been used by the media, in the context of bee biology and its interactions with the environment. The impact of my research on media has been considerable, and has helped publicising the importance of fundamental research for our understanding of the natural world and the way it works. Other impacts are starting to be felt, in instrumentation development and application to assessing electric field in the living environment.
First Year Of Impact 2014
Sector Education,Electronics,Environment,Healthcare
Impact Types Cultural,Societal,Economic

 
Description ERC Advanced Investigator Grant
Amount £2,400,000 (GBP)
Organisation European Union 
Sector Public
Country European Union (EU)
Start 09/2017 
End 08/2022
 
Description Royal Society Newton International Exchange
Amount £12,000 (GBP)
Organisation The Royal Society 
Sector Academic/University
Country United Kingdom
Start 03/2015 
End 04/2017
 
Title Finite element modelling - Multiphysics modelling 
Description This method is standard within the engineering and physics community. It is increasingly used in the life sciences, as software is becoming available and amenable to the complexity of biological systems. Also, a large portion of accessibility is due to the power of modern desktop computers. 
Type Of Material Model of mechanisms or symptoms - non-mammalian in vivo 
Provided To Others? Yes  
Impact The method has impacted on our capacity to model the complex interaction of organisms with their physical environment. This aspect - that we call Physical Ecology - is expanding and is poised to touch many realms of life Sciences. For us the impact has been significant as the model predictions have allowed us to better understand the sensory ecology of the organisms we study, mostly insects, but also plants. 
URL https://uk.comsol.com/
 
Title Laser Doppler vibrometry applied to plant samples 
Description This is a new application of the technology, applied to measuring small vibrations on plant samples. - namely seeds, and seedlings. 
Type Of Material Biological samples 
Year Produced 2008 
Provided To Others? Yes  
Impact Our research has now established that vibrations at the level of picometers (10 to the minus 12) can be measured on seeds and seedlings. The full impact is not realisable yet, but we have good evidence to say that it may be useful to measuring the viability of any individual seed. Could have impact in agriculture, if made practical and cheap a technique. Now it is expensive and a rather specialised technique. 
 
Title Photo Multiplier tube 
Description This technique has been around for a while and in its most expanded form is used to detect neutrinos crossing the earth. Here, we apply a much reduce, cheaper and simpler version to measure the photons emitted by plant material. As a plant grows it emits photons (in fact every thing does when disturbed mechanically). We are measuring photon emissions in conjunction with growth of seeds and seedlings. Only a few labs have been doing so, and we have good reason to think that this technique is very promising, in tandem with laser Doppler techniques as well. 
Type Of Material Biological samples 
Year Produced 2010 
Provided To Others? Yes  
Impact Health monitoring in seeds, detection of gravitational variation in plants. 
 
Title Predictive models of bee activity and weather 
Description The model provides a statistical tool and analysis method that enables the prediction of activity of honeybees as a function of simple meteorological variables. 
Type Of Material Computer model/algorithm 
Year Produced 2017 
Provided To Others? Yes  
Impact Thus far, there has not been a noticeable impact of this method. There has not been many seasons' worth of applicability of this method, and as our funding on this has run out, we are not in possession of continuous data anymore. 
URL https://doi.org/10.1007/s1592-018-0565-3)
 
Description C. Gallep - UNICAMP Sao Paulo 
Organisation State University of Campinas
Country Brazil 
Sector Academic/University 
PI Contribution The partnership is between Prof Cristiano Gallep from Sao Paulo UNICAMP, an expert in biophotonics and ultraslow photo emissions in biological material. Our contribution is towards the development of a novel approach in assessing the function of photonics emissions, marrying photon detection (Gallep) to nano mechanics (Robert). In brief, simultaneous measurements using photon detectors (PMT) and laser Doppler vibrometry, AFM and KPFM, will be used to establish causation and correlations between physiological processes and biophotons and vibrations. We contribute time and expertise. The partnership benefits from reciprocity complementarity, as the respective expertises are at first sight unlikely yet find a use and "raison d'être" in a common question and hypothesis setting. This partnership is funded by a Royal Society Newton Exchange programme (finished) and a BBSRC UK-Brazil partnership award (ongoing).
Collaborator Contribution Partners are contributing time and expertise in biophotonics, in the context of the home department of electrical engineering in Limeira/Sao Paulo. See above for more details of reciprocal benefits
Impact Collaboration is multidisciplinary, involving engineering and biology; more precisely electrical engineering, optical telecommunication engineering, sensory biophysics, nano mechanics, botanics, crop science and insect science.
Start Year 2017
 
Description Collaboration with Dr. Martin Fullekrug, University of bath 
Organisation University of Bath
Department Department of Physics
Country United Kingdom 
Sector Academic/University 
PI Contribution Understanding of the importance of atmospheric electricity to animal species at the small scale of the biometric range. Development of biophysical tests and psychophysical tests to better understand aerial electroreception. The interdisciplinary partnership meets in the territory of atmospheric electricity and its elusive effects on biological organisms.
Collaborator Contribution Development of a better understanding of atmospheric electricity and its dynamics, and presence around object in mid-air and near to the ground. Ground based or plant based electrostatics and atmospheric potential gradients are elusive quantities.
Impact Yearly participation to the CTR Wilson meeting - poster and talk presentations. Many meetings and lab visits, project development, instrumentation development.
Start Year 2016
 
Description Dr. Tim Helps - electric sensors and actuators 
Organisation University of Bristol
Department Department of Electrical and Electronic Engineering
Country United Kingdom 
Sector Academic/University 
PI Contribution Setting up the context and constraints of low level electric sensors that are self powered and self-calibrating. This is a bio-inspired approach on electroreception, that exploits the reciprocity effects between sensors and actuators. Interestingly, the sensor-actuator issues on electric mode is very similar, if not analogous to that encountered by my group and me in the past 25 years of research in active hearing.
Collaborator Contribution The partners are providing know-how and defining the questions from the actuator side of the problem. The sensor-actuator system will rely on existing but scaled down technology developed for electro gel actuators. The Bristol team are world leaders on these systems.
Impact No output yet. We are aiming for a large impact paper and application
Start Year 2018
 
Description Electro-Photonics - M. Cifra 
Organisation Academy of Sciences of the Czech Republic
Country Czech Republic 
Sector Learned Society 
PI Contribution Contribution research questions and techniques to measure local electrical potentials and charges on biological surfaces.
Collaborator Contribution Contribution to developing technique to asses the physiological dynamics of electrosensitive bio-surfaces, using photons. Access to cellular level mechanisms of electro photonic effects.
Impact none so far in terms of publications - in prep
Start Year 2016
 
Description Electrometer for bees/insects - Kerry Nicol 
Organisation University of Bath
Country United Kingdom 
Sector Academic/University 
PI Contribution Research question, funding. Electrode design, parameter space and design constraints.
Collaborator Contribution Unique technology pertaining to the design of sensitive electrometer that can measure weak potentials around complex biological structures.
Impact none yet
Start Year 2015
 
Description Bristol festival of Nature 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? Yes
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Festivals produce all sorts of results, many of them will not be measurable. Yet, the instant feedback we experience from the audience, from the visitors, ells us about their amazement at the beauty and complexity of the biological world. When bees are concerned, which is one of the themes of research we pursue and present in public engagement, the awareness of the visitors is very much alive; our contribution is to enrich the context of their knowledge on bee biology, life history and uncertainty for the future. Outcomes encompass invitation to speak at the Bristol Scientific Cafe at the Tobacco Factory Cultural Center, the Bristol Science Club, the British Beekeeper's association, and give interviews to the press and television.

Impacts of this activity are sometimes measured by the pupillary and eyelid expansion, and level of yaw dropping in pupils. Many pupils from schools in and around Bristol have convinced us that they are fascinated by biology. Because we present science at the interface between Physics and biology, we reach areas of connections that are not necessarily made in the classroom. We have witnessed the realisation in many pupils that one can do cool physics by studying biology, and the reverse as well. Quite satisfactorily, their teachings think the same and ask for material to incorporate into their lectures.
Year(s) Of Engagement Activity 2010,2011,2012,2013,2014
URL http://www.bnhc.org.uk/festival-of-nature/
 
Description David Attenborough's Natural Curiosities 
Form Of Engagement Activity A broadcast e.g. TV/radio/film/podcast (other than news/press)
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Media (as a channel to the public)
Results and Impact On two occasions, our research was featured in Sir David Attenborough's Natural curiosities. Other TV channels also did some pieces, notably Arte and Canal+.
Year(s) Of Engagement Activity 2015
 
Description Interview for National news 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Media (as a channel to the public)
Results and Impact There were several interviews with media, in fact several dozens, as our paper on Bee electroreception came out. Upon publication of the next articles, in 2016, 2017, and 2018, numerous outlets took up the news to produce updates on the story. Several social media were conveying the news, and thousands of tweets ensued.
Year(s) Of Engagement Activity 2015,2016,2017,2018
 
Description Open Days UCAS 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? Yes
Geographic Reach National
Primary Audience Undergraduate students
Results and Impact Recruitment of students

Recruiting quality students and provide them with the motivation that our institution is the one where to learn biology.
Year(s) Of Engagement Activity Pre-2006,2006,2007