The bee, the flower, and the electric field: electric ecology and aerial electroreception

Abstract

Bees and flowering plants have a long-standing and remarkable co-evolutionary history. Flowers and bees evolved traits that enable pollination, a process that is as important to plants as it is for pollinating insects. From the sensory ecological viewpoint, bee-flower interactions rely on senses such as vision, olfaction, humidity sensing, and touch. Recently, another sensory modality has been unveiled; the detection of the weak electrostatic field that arises between a flower and a bee. Here, we present our latest understanding of how these electric interactions arise and how they contribute to pollination and electroreception. Finite-element modelling and experimental evidence offer new insights into how these interactions are organised and how they can be further studied. Focussing on pollen transfer, we deconstruct some of the salient features of the three ingredients that enable electrostatic interactions, namely the atmospheric electric field, the capacity of bees to accumulate positive charge, and the propensity of plants to be relatively negatively charged. This article also aims at highlighting areas in need of further investigation, where more research is required to better understand the mechanisms of electrostatic interactions and aerial electroreception.

Full text

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J Comp Physiol A (2017) 203:737–748
DOI 10.1007/s00359-017-1176-6
REVIEW
The bee, the flower, and the electric field: electric ecology
and aerial electroreception
Dominic Clarke1 · Erica Morley1 · Daniel Robert1
Received: 15 December 2016 / Revised: 26 April 2017 / Accepted: 27 April 2017 / Published online: 24 June 2017
© The Author(s) 2017. This article is an open access publication
Introduction
Animal pollinators detect and select flowers by their col-
ours, shapes, patterns, fragrant volatiles (Raguso 2008),
and, in some cases, temperature (Rands and Whitney 2008)
and tactile cues (Kevan and Lane 1985). Some plants can
signal to their pollinators using corolla air humidity (von
Arx et al. 2012) and even using acoustics, as some bats
use floral echoes to localize nectar resources (Simon et al.
2011). The diversity of animal pollinators, and the vari-
ety of pollination syndromes, is vast (for a comprehensive
review, see Willmer 2011). While bees carry out fewer total
flower visits than other pollinators, they are responsible for
about half of all crop pollination (Rader et al. 2016). The
relationship between bees and flowers constitutes a com-
plex example of co-evolutionary adaptation, whereby the
interests of both parties are served. Flowers use bees as
vehicles to enhance pollen transport and fertilization, while
bees greatly benefit from pollen and nectar as food sources
(for a recent review, see Nicholls and Hempel de Ibarra
2017). This co-evolutionary relationship turns out to be
rich and complex. It involves cooperation between plants
and their animal vectors, to the benefit of each, but also
involves competition and adaptive compromise. For exam-
ple, the nectar reward is expensive for the plant to produce.
In milkweed, up to 37% of the daily photosynthetic energy
is spent producing nectar reward for pollinators (South-
wick 1984), energy that is no longer available to the plant.
However, a more energetic reward is likely to attract more
pollinators, forcing a trade-off. Literature on the subject is
very rich and diverse, exploring the complexities of plant-
pollinator interactions, and the diverse strategies and adap-
tations for plant reproduction and insect foraging (Chittka
and Thomson 2001). Here, we present an aspect of plant–
pollinator interactions that has been underappreciated thus
Abstract Bees and flowering plants have a long-standing
and remarkable co-evolutionary history. Flowers and bees
evolved traits that enable pollination, a process that is as
important to plants as it is for pollinating insects. From
the sensory ecological viewpoint, bee–flower interactions
rely on senses such as vision, olfaction, humidity sensing,
and touch. Recently, another sensory modality has been
unveiled; the detection of the weak electrostatic field that
arises between a flower and a bee. Here, we present our lat-
est understanding of how these electric interactions arise
and how they contribute to pollination and electroreception.
Finite-element modelling and experimental evidence offer
new insights into how these interactions are organised and
how they can be further studied. Focussing on pollen trans-
fer, we deconstruct some of the salient features of the three
ingredients that enable electrostatic interactions, namely
the atmospheric electric field, the capacity of bees to accu-
mulate positive charge, and the propensity of plants to be
relatively negatively charged. This article also aims at high-
lighting areas in need of further investigation, where more
research is required to better understand the mechanisms of
electrostatic interactions and aerial electroreception.
Keywords Bees · Plants · Electric fields · Pollen ·
Mechanoreception
* Daniel Robert
d.robert@bristol.ac.uk
1 School of Biological Sciences, University of Bristol, Life
Science Building, 24, Tyndall Avenue, Bristol BS8 1TQ, UK
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738 J Comp Physiol A (2017) 203:737–748
1 3
far: the presence of electrostatic forces between bees and
flowers. We describe how and why these electric fields
exist, the mechanism by which bees detect weak aerial
electrostatic forces and the function of these forces in pol-
len transfer (Fig. 1a).
Detection of weak electric fields in air by bees
Electroreception, defined as the ability of an organism to
detect external electric forces, has long been known in
animals living in aquatic, electrically conductive environ-
ments, for example, in fish (Kalmijn 1971; Bullock and
Heiligenberg 1986), in amphibians (Hurd et al. 1984), and
in platypus (Gregory et al. 1987). Although electrorecep-
tion in an aerial environment had previously been hypoth-
esised in bees (Yes’kov and Sapozhnikov 1976; Corbet
et al. 1982), only recent studies have provided behavioural
and physiological evidences for the phenomenon (Clarke
et al. 2013; Greggers et al. 2013; Sutton et al. 2016). So
far, evidence points to detection mechanisms for aerial
electric forces that are very different from those described
in aquatic animals (Bullock and Heiligenberg 1986). In
aquatic animals, electroreception relies on direct trans-
mission of stimulus from the conductive medium (water)
to the nervous system, via conductive receptor channels
(ampullae of Lorenzini). For terrestrial animals residing in
air, an electrically resistive medium, detection of electric
fields must operate differently and constitute a new sensory
capacity.
Bumble bees, Bombus terrestris (Clarke et al. 2013)
and honey bees, Apis mellifera (Greggers et al. 2013)
have been shown capable of detecting weak electric fields,
each in different behavioural contexts, using different sen-
sory mechanisms. Bumble bees can sense the presence of
weak electric fields (e-fields) surrounding flowers, and dis-
criminate between e-fields with different radial geometries
(Clarke et al. 2013). The sensory basis for e-field detection
in bumble bees appears to rely on mechanosensory hairs,
which are mechanically deflected by an applied electric
stimulus (Sutton et al. 2016) (Fig. 1b, c). The mechanical
deflection of these hairs in turn elicits neural responses,
conveying information to the bee’s central nervous system.
Using laser Doppler vibrometry (a technique that meas-
ures nano-scale vibrations), the deflection of a series of
dorsal hairs in response to applied electric fields reveals a
collective sensitivity covering a range of stimulus frequen-
cies (Fig. 1c).
Bumble bees can use electric information to discrimi-
nate between rewarding and unrewarding flowers (Clarke
et al. 2013). They can also learn colour discrimination tasks
faster when colour cues are paired with electric field cues
similar in magnitude to those surrounding natural flowers.
In effect, bumble bees did not learn as readily in an elec-
trically neutral environment (Clarke et al. 2013). This evi-
dence establishes that electric fields are part of the sensory
Fig. 1 Electromechanical reception in bumblebees and electrical
ecology of pollination. a Interactions between bee, flower, and atmos-
pheric electric field cannot be separated, as each of them influence
the other. b Frontal confocal photograph of a bumble bee illustrating
target hairs used to establish the site of electromechanical detection
of electric fields in bumble bees (modified from Sutton et al. 2016). c
Mechanical response of diverse bumble bee hairs to an electric field
stimulus. Vibration velocity v elicited by a multifrequency electrical
stimulus (0–10 kHz) was measured using laser Doppler vibrometry.
Each line represents a measurement of a single hair from different
animals (N = 12). Hair displacement d as a function of frequency f is
given by d = v/πf
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739J Comp Physiol A (2017) 203:737–748
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experience of foraging bees, one of the many, multimodal
floral cues. It seems, therefore, that floral e-fields are used
to inform foraging behaviour in bumble bees. Honey bees
reportedly use electroreception for intraspecific communi-
cation, utilising their antennae in e-field detection (Greg-
gers et al. 2013). Unlike bumblebees, returning honey bee
foragers perform a waggle dance, which communicates
details of food sources to other conspecifics within the
hive (von Frisch 1954). In addition to sensory cues in other
modalities, low-frequency oscillating electrical stimuli are
produced by electrically charged vibrating foragers as they
perform the waggle dance. Honey bees are sensitive to
these stimuli (Greggers et al. 2013).
The sensory basis for electroreception in honey bees
was hypothesised to be the antennae, electro-mechanically
coupled to the surrounding e-field in virtue of bees being
electrically charged, and thus subject to electrostatic forces.
Transduction of these forces was proposed to be taking
place in the antennal Johnston’s organ (Greggers et al.
2013). Greggers et al. (2013) demonstrate that honey bee
antennae oscillate under electric field stimulation, and this
stimulation can elicit activity in the antennal nerve. It was
also shown that honey bees with removed or fixed anten-
nae are less able to associate food reward with electric field
stimuli within a classical conditioning paradigm. Investi-
gating the sensory basis for electroreception in bumblebees,
it was shown that the electromechanical sensitivity (i.e.,
velocity and angular displacement in response to electric
field stimuli) of bumble bee hairs is considerably greater
than that of their antennae (Sutton et al. 2016). The sen-
sitivity of these hairs to a wide variety of stimulation was
reported in direct comparison with the antennae of the same
individual bees. Hairs were shown to move with roughly
an order of magnitude greater velocity and 3–4 orders of
magnitude greater angular displacement than antennae
across a broad frequency bandwidth. Peak response of the
hairs typically occurred at stimulus frequencies between 2
and 4 kHz, consistent with the low mass and high stiffness
of the hairs. The minimum electric field required to pro-
duce measurable deflections in the hairs was between 0.77
and 61 V/m depending on stimulus frequency. Antennae
required larger minimum field strengths of between 15.3
and 306 V/m. Extracellular recordings from the base of the
hairs in 15 individual bumble bees show increased neural
activity accompanying electric field stimuli even at low fre-
quencies (<1 Hz) (Sutton et al. 2016).
In both hairs and antennae, the mechanism of elec-
tric field detection in bees is thought to be the same: a
rigid cantilever, projecting from the body, carrying an
electric charge, subject to external electric force, with a
sensitive force-transducer at the base. The motion of both
of these structures is lever-like, where the whole struc-
ture displaces in constant phase with linearly increasing
amplitude from base to tip, and minimal bending (see
supplementary materials for Sutton et al. 2016). This
arrangement simultaneously maximises the electric
charge density at the tip of the lever (increasing electro-
static force at the tip) and the moment arm of the force
with respect to the fixed base of the lever. Therefore, it
seems that although bumble bees and honey bees can
both detect weak e-fields, they do so using different but
physically analogous electromechanical systems.
Neither mechanosensory hairs nor antennae are unique
to bees. It is, therefore, possible that other arthropods also
use these structures to detect electric fields. Mechanosen-
sory structures in insects have previously been shown to be
involved in detection of various fluid-mechanical signals,
by a diverse range of arthropods (Casas and Dangles 2010).
These signals include the air displaced by moving prey
or predators, or the air flowing over the body of the ani-
mal during flight. Mosquitoes use their antennae to detect
sound particle velocity in lieu of tympanal organs for audi-
tion (Göpfert et al. 1999). In the case of fluid-mechanical
signals, the signal source must be viscously coupled to the
sensory structure through the medium. In the case of elec-
troreception, the signal source is directly electrically cou-
pled to the sensory structure through the electric field. Fur-
thermore, electric field detection is not subject to the same
boundary layer constraints that influence fluid-mechanical
signal detection (Casas and Dangles 2010). Both elec-
troreception and fluid-flow detection are comparable, and
indeed, electrostatic actuation has been used to generate
deflections of the particle velocity and fluid-flow sensors
in fruit flies and scorpions (Hoffmann 1967; Albert et al.
2007). Electrical stimuli elicit a neural response from hair
deflections of 0.04° in bumble bees (Sutton et al. 2016).
Minimum sensitivity thresholds have yet to be established.
This is within the same order of magnitude as cricket fili-
form hair sensitivity, which shows neural responses to hair
deflections of 0.02° (Shimozawa et al. 2003). This suggests
that electroreception by mechanosensory hairs or antennae
is no more demanding a sensory task than fluid-flow detec-
tion by the same structures.
Electroreception by hairs and antennae needs not to
be mutually exclusive. This sensory ability may be called
upon in different behavioural and ecological contexts,
either by different species in different environments, or by
individuals performing different roles within and outside
the hive. For all currently known examples of aerial elec-
troreception, the exact nature of the information transferred
remains elusive. However, the results of the above-cited
experiments (Clarke et al. 2013; Greggers et al. 2013; Sut-
ton et al. 2016) point to the possibility that bees can detect
and use aerial electric fields in the contexts of foraging and
in-hive communication over short distances (none of the
above studies demonstrate e-field detection at distances
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740 J Comp Physiol A (2017) 203:737–748
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higher than 10 cm). Other behavioural functions are not
excluded, but have yet to be investigated.
Unveiling the nature of electric ecology
Understanding any sensory system requires not just a
description of ability with an associated sensory structure,
but a detailed understanding of the external stimuli in the
environment of the organism. The structure, distribution,
and abundance of information available to an organism are
of comparable importance to that of energy and reproduc-
tive opportunity. For vision, a great deal is known about
both the physiological underpinnings of the sense, and
the world of external stimuli relevant to it (Cronin et al.
2014). This is also true of audition and olfaction (Barth
and Schmid 2001). For aerial electroreception, the picture
is less well developed. Relatively little is known about
the structure and dynamics of electric fields and electric
charges at the spatiotemporal scale of flowers and bees.
This is a scale which is too large and heterogeneous to
describe in precise mathematical terms and too small to
measure accurately with the conventional equipment, espe-
cially in the context of field biology. Furthermore, the con-
ventional electronic measuring equipment does not perform
well when applied to extremely high impedance measure-
ment regimes such as measuring electric fields in air. That
is to say that there is no good equivalent of the camera
or the microphone to acquire spatially resolved static or
dynamic information about weak electric fields and their
interactions with living organisms.
In the following sections, we present our current under-
standing of the interactions between the bee, the flower,
and the aerial electric field, and spell out some emerging
questions. How and under which circumstances do elec-
tric fields arise in the environment and around living mat-
ter? How and why can these fields be relevant for sensory
detection and perception? What are the signals being sent
and received by organisms within this modality? What are
the magnitudes of the forces involved? What environmental
factors affect the proper functioning of this sense? Can we
effectively describe the dynamic electrical environment of
plants and their pollinators?
The electric field: atmospheric electricity and the
atmospheric potential gradient
The atmospheric potential gradient (APG) is the term given
to the vertical electric field that exists between the earth
and the upper atmosphere (reviewed in detail in Rycroft
et al. 2000, 2012). The APG is of great importance to the
electrical ecology of biological systems, as will be outlined
below and in the following sections. To understand its
effects on plants and animals, we first provide a brief over-
view explaining the APG itself.
The electric field strength at the surface of the earth, in
a flat, open region, in fair weather, is of the order of 100 V
for every 1 m gained in altitude (~100 V/m). This increase
in voltage continues towards a maximum of around 300 kV
at an altitude of 30–50 km, above which the potential
begins to decrease and invert (Beach and Rines 1904). This
potential gradient is maintained globally by the action of
electrical storms taking place around the earth. The cur-
rent that flows down to earth in the fair weather field is
exactly balanced by lightning strikes moving charge in the
opposite direction elsewhere on the planet (Rycroft et al.
2000, 2012). Collectively, these processes are known as the
global atmospheric electric circuit. In response to the posi-
tive potential of the air, negative charge accumulates on the
surface of the earth. This charge accumulation results from
electrostatic induction, whereby a charged object external
to a conductor induces the opposite charge to move to that
conductor’s surface, proximal to the external charge (Fey-
nman et al. 1964). This charge accumulation cancels out
the electric field inside the conductor. Likewise, negative
charges inside the earth accumulate on the surface to cancel
out the 100 V/m field just above the surface. The surface of
the earth behaves rather like a single plate of a capacitor,
where the opposite plate is the high-voltage layer of upper
atmosphere and the dielectric is the air. Any object that is
conductively linked to earth accumulates negative charge at
its surface in this way. The further into the field this object
extends, the greater the potential difference between its
upper surface and the surrounding air (~100 V for every
meter). This effect results in large concentrations of charge
that, in turn, produce their own electrical forces, generat-
ing local distortions in the otherwise uniform atmospheric
electric field (Fig. 2).
Using a mathematical model, 5 m tall trees growing on
flat ground are shown to produce substantial alterations in
the electric field strength in the surrounding air. The posi-
tive charge in the atmosphere draws a negative charge to
the surface of the trees (Fig. 2, inset). Notably, sharp
extremities and spikes produce larger fields than shallow
curves or flat surfaces. This is because the charge den-
sity at the surface of a conductor is inversely proportional
to the radius of curvature of that surface (Feynman et al.
1964). The higher the charge density at a point, the larger
the electric field is around this point. In effect, local distor-
tions to the APG caused by grounded objects are not only
influenced by object height, and APG strength, but also
very much by the geometry of the object. These effects also
apply at smaller scales. At the scale of the flower, we name
the local distortions in background e-field around a flower,
the “floral electric field” (Clarke et al. 2013). This is the
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741J Comp Physiol A (2017) 203:737–748
1 3
scale at which bees are acting and interacting. Understand-
ing the dynamics of electric fields at this scale is, therefore,
essential to understanding the electric sense of bees and the
electrical signalling of flowers.
The Bee: the role of the triboelectric effect
Bees are not electrically connected to the earth, like flow-
ers are, yet they also gain a charge as they fly through the
air. The acquisition and maintenance of charge on a bee is
a key factor in their ability to detect electric fields (Sutton
et al. 2016), with just slight increases in charge causing
large gains in electromechanical sensitivity of both hairs
and antennae. It is also crucial to intraspecific electrical
communication in honey bees; the dancing bee must be
charged to convey electrical signals to fellow bees within
the hive (Greggers et al. 2013). A bee’s bulk charge will
also induce stronger electrical interactions between itself
and any flower it visits, strengthening electrostatic forces
on pollen. The mechanism by which bees gain their charge,
however, is not well understood.
The triboelectric effect is the name given to the phe-
nomenon of materials either taking on or giving up elec-
trons upon frictional contact with a different material, thus
becoming negatively or positively charged, respectively.
Each material can be placed on a series, with more posi-
tive-going materials at one end and more negative-going
materials at the other. This is called the triboelectric series.
While the phenomenon is somewhat variable and difficult
to quantify, the relative position of a large number of syn-
thetic and organic materials on this series is fairly well
understood (Diaz and Felix-Navarro 2004). Walking insects
have been shown to gain charge through friction between
their bodies and the surface on which they walk (Edwards
1962). By measuring the polarity of these charges, Edwards
(1962) was able to determine that insects have a propensity
to gain a positive charge upon frictional contact with vari-
ous materials, placing them on the positive end of the tribo-
electric series along with other biological materials such as
human skin and cat fur.
The tendency of bees to become positively charged is
well evidenced (Erickson 1975; Vaknin et al. 2000; Clarke
et al. 2013). This charge generates forces on other charged
objects in the vicinity of the bee from flowers to the elec-
troreceptor hairs and antennae of conspecifics. The net
charge on the bee was measured as between around +30
and +50 pC depending on the particular study, and genus.
The size and shape of bees suggest a very low capacitance
(~pF), such that surface voltage would be of the order of
hundreds of volts (Yes’kov and Sapozhnikov 1976; Cor-
bet et al. 1982). If the charge was concentrated in certain
areas (e.g., sensory structures like hairs and antennae), this
potential could be much greater. It is a reasonable hypoth-
esis that triboelectric interactions play a role in this charg-
ing. The high-energy motion of flight is met with friction
from the air and between various surfaces on the bee itself.
To determine the triboelectric rank of bees, we have con-
ducted a similar experiment to Edwards (1962), rubbing
the dorsal surface of freshly killed bees against various
Fig. 2 Finite-element model of the atmospheric potential gradi-
ent (APG) and its interaction with plants. Background colour shows
strength of the electric field as a function of altitude from ground
(scale inset). The positive ionospheric charge is included, located
between 60 and 100 km above ground (not to scale). Local distortions
in the uniform APG, caused by the presence of the trees, are labelled.
The approximate space charge density is shown inset. The APG
induces negative charges to build up on the surface of the ground and,
in higher density, on the upper surfaces of the trees, which, in turn,
induce opposite charges in the surrounding air
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742 J Comp Physiol A (2017) 203:737–748
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materials, both synthetic and natural. We included several
materials that are often found at the most positive end of
the series like rabbit fur and polyurethane foam. We also
used various other materials that occupy positions across
the series from positive to negative. Before each meas-
urement, bee charge was zeroed, and then, the bees were
manually rubbed along a 10 cm strip of material, ten times
each, at which point the charge on the bee and the material
were both measured using a Faraday pail as in Clarke et al.
(2013). Measurements were carried out at 50% relative
humidity and 20 °C, and each measurement was repeated
ten times. We were unable to identify a material that caused
the bee to gain a negative charge, placing the bee at the far
positive end of the series (Fig. 3). Edwards’ (1962) results
on moths, beetles, and flies reveal the same tendency for
insect cuticle to charge positively, where only asbestos
(not available in our experiments) became more positively
charged than the insects.
The results of the triboelectric experiments raise several
questions: Is the tendency to become positively charged
generic to all flying insects, or does it constitute an adapta-
tion particular to bees or pollinators? Triboelectric charging
is not simply a function of the material’s intrinsic electrical
properties, but also of surface morphology which affects
the contact surface area undergoing friction. Is the insect
cuticle physically adapted to maximise or modulate this
effect? Does charge separation or equalisation take place
when bees experience contact and friction against flowers
that have conductive connections to ground? All of these
questions pose difficult experimental challenges that have
not been fully addressed.
The flower: floral electric field
An aesthetic if not quantitative way of visualising the pres-
ence of an electric field around a flower can be achieved
by dusting natural flowers with electrostatically charged
coloured powder (Clarke et al. 2013). The structure of the
electric field near to the surface of a flower is revealed by
the selective deposition of coloured charged dust (Fig. 4).
Some details of floral anatomy are highlighted with notice-
ably larger paint deposition, whereby the parts of the flower
with higher charge density (and therefore greater electric
force) tend to be along contours and sharp features, such
as the edges of petal, stigma, and anthers, but also small
features such as the trichome (Fig. 4). This method of visu-
alising heterogeneity in floral charge density highlights the
possibility that flower anatomy plays a role in building a
structured electric field. In turn, this opens up questions
about the actual, species-specific electrical characteris-
tics (e.g., conductivity and capacitance) of different floral
organs and their potential role in insect/flower interactions.
The difference in charge density between different struc-
tures can be thought of as electrical “contrast”. The geom-
etry of petal edges, where charge density is high, provides
spatial structure to the floral field, giving it an outline.
There is further contrast between the flat petal surfaces and
the protruding trichomes, stigma, and anthers. Just like they
display spectacular corolla adaptations for certain pollina-
tion syndromes, different plant species may employ differ-
ent strategies in the way they organise their electrostatic
floral footprint, to make themselves electrically distinc-
tive to potential pollinators. Spiked flowers such as teasels
Fig. 3 Position on the tribolelectric series of various materials,
including bumble bees and rabbit fur. Y-axis shows the position of
each material according to available literature (Diaz and Felix-Nav-
arro 2004). Materials shown are rabbit fur, polyurethane foam (PU),
nylon, paper, cotton, high-density polyethylene (HDPE), polytetra-
fluoroethylene (PTFE), and polyvinyl chloride (PVC). Those at the
top (red, positive) end tend to lose electrons during frictional contact
with other materials, becoming positively charged. Those at the bot-
tom (blue, negative) tend to gain electrons and become negatively
charged. The x-axis shows the difference in charge of the material
(light blue) and a bumble bee (red) after rubbing the material on the
dorsal surface of the bee. The grey and black striped bars show the
bee charge minus the material charge, giving the total charge trans-
ferred triboelectrically during the rubbing. No material caused a bum-
ble bee to become negatively charged after contact, placing the bee at
the most positive end of the triboelectric series along with rabbit fur.
Each datum shown is an average of ten repetitions of the measure-
ment
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743J Comp Physiol A (2017) 203:737–748
1 3
(Dipsacus sp.) should have a distinct pattern of electrical
contrast from a petunia (Petunia sp.) for example, and like-
wise, a raceme will have a different electrical contrast to an
umbel inflorescence. Features with sharp edges or points,
both within a flower (anthers, stigma, petal edges, etc.) or
on the overall plant (racemes, single protruding blooms),
should have a stronger electric field purely due to their
geometry.
Computer simulation can help quantify electrical forces
without the need for direct measurements. In particular,
finite-element analysis (FEA) allows the partial specifi-
cation of a physical situation using empirical data, which
can then be used to calculate many difficult or impossible
to measure features of that situation. For aerial electrore-
ception, these models stand in where direct measurement
of the electric field is unavailable, providing a description
of how the morphology and material properties of flowers
and bees interact to induce forces on one another, and on
charged objects in their vicinity. In Fig. 4, we show a model
of positively charged bumble bees, flying in the vicinity
of Petunia flowers rooted in the ground. While this model
is simplified for illustration, the simulation is still empiri-
cally specified, with plant material properties, bee charge,
and atmospheric electrical conditions taken from available
literature. These 2D models are easily generalised to 3D
(Clarke et al. 2013), with the biggest challenge being the
specification of the intricate 3D geometry of flowers.
In this model (Fig. 4), the colour of the air shows the
magnitude of the electric field vector at that point in space.
Contour lines are lines of constant electric potential. Where
they are close together, the electric field strength is high.
The strongest electric fields arise as a bee approaches close
to a flower. The bee carries a positive charge that it acquires
while flying (Colin and Chauzy 1991; Clarke et al. 2013).
The flower gains a negative charge through electrostatic
induction. The forces that exist between charges fall off
with the square of their distance (Feynman et al. 1964),
so that the forces between bee and flower increase quickly
as the bee approaches. At a distance of 2–3 cm shown in
Fig. 4, the region between the bee and the flower has an
electric field of over 5 kV/m. This is comparable in mag-
nitude to the electric field at the ground under a high-volt-
age power line. This field strength is much higher than that
required to elicit mechanical and neural responses from
bumble bee hairs (Sutton et al. 2016). Hence, forces that
produce detectable fluctuations in bee hairs arise at several
body lengths away from the flower. These are the forces
that bees can detect to assess floral rewards.
With currently available instrumentation, it is not pos-
sible to directly measure the computed quantities with as
good a spatial or temporal resolution as that provided by
finite-element analysis. A further benefit conferred by the
finite-element analysis is that it allows experimenters to
quickly explore the wide parameter space that exists within
the specification of the model, changing and tweaking
many aspects of it and comparing the results of thousands
of simulated experiments. This can be extended from 2D
Fig. 4 Experimental visualisation of floral electric field using elec-
trostatic dusting. Flowers are shown before (left) and after (right)
dusting with positively charged coloured powder (blue or yellow on
the bottom image). Genera shown are a Lilium, b Gerbera, c Narcis-
sus, d Bergenia, and e Petunia. Heterogeneous powder deposition
reveals spatial differences of charging in the flower, with higher levels
of deposition corresponding to points of greater negative charge den-
sity on the flower. The principal determinant of shape and strength of
the floral electric field is flower geometry. Flowers were connected to
electrical ground and no APG was experimentally imposed
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744 J Comp Physiol A (2017) 203:737–748
1 3
into 3D, and from stationary to dynamic, time-domain, and
frequency-domain studies. Ultimately, a dynamic represen-
tation of the electrical scene involving flying bees, growing
plants, and an ever-changing atmospheric potential gradient
could be constructed.
Interactions on smaller scales: electrostatic pollen
transfer
During the bee’s final approach to the flower, electro-
static forces between these two bodies grow rapidly larger
(Fig. 5). This has been suggested to have important con-
sequences for pollen transfer from anther to bee and back
from bee to stigma (Corbet et al. 1982; Erickson and Buch-
mann 1983; Vaknin et al. 2000, 2001). In addition, indeed,
electrostatic pollen transfer can be demonstrated experi-
mentally by bringing a charged acrylic rod in close vicinity
to a pollen-bearing stigma (Fig. 6). In this experiment, bidi-
rectional transfer from anther to charged rod and charged
rod to stigma is clearly apparent, and depends upon the
polarity of applied charge.
Just as morphology, geometry and specific impedance
of structures are key influences on the electric field at the
scale of trees and plants (Fig. 2), this remains true at the
smaller scale of a flower’s anther, stigma, and pollen grain.
Simply due to their geometry, protruding floral structures
such as a long stigma will create a strong local electric field
(Fig. 7a, b), and indeed, flowers with a flat corolla and long
stigma appear to capture more pollen through electrostatic
forces than those with concave corolla and shorter stigma
(Vaknin et al. 2001). However, the specific impedance and
connectivity to electrical ground will also influence the
electric field around different floral components. Measure-
ments from oil seed rape flowers (Brassica napus) show the
stigma and outer nectaries to have lower impedance paths
to earth than the petals, sepals, styles, and anthers (Corbet
et al. 1982), resulting in relatively greater charge density by
induction at these points (Fig. 7a, b).
Knowing that electrostatic forces can influence pol-
len transfer (Fig. 6) and that morphology, conductivity,
and overall geometry influence the forces generated, how
can we best describe their impact on pollen transfer in the
flower–bee interaction? The modelling approach, again,
has yielded the greatest insights so far. Bowker and Cren-
shaw (2007a, b) analytically modelled the motion of pollen
charged to between 0.1 and 40 fC as it falls under grav-
ity and determine that electrostatic forces can cause plants
to draw in and capture pollen that would otherwise be lost
under the influence of gravity, from significant distances
away (cf >20 mm for pollen carrying 10 fC of charge).
We have here constructed another quantitative model,
Fig. 5 Visualising electric ecology. Finite-element model of electric
interactions between positively charged bumble bees and grounded
petunias (Petunia sp.) against the background of the atmospheric
potential gradient. Bees are modelled as a simplified silhouette of
their body shape—ignoring the fine structure of their appendages and
hair cover. Total bee charge was taken as 32 pC, unevenly distributed
on its surface area, with higher charge densities on high curvature
areas, such as the head, wings, and abdomen. Petunias are modelled
as slightly electrically conductive bodies that are grounded to earth
(resistivity ~10 MΩm). Model petunias are constructed to mimic
their natural shape. The electric field strength is encoded as the col-
our of the air domain (see scale bar, bottom-centre), and contour
lines show every 10 V interval in electric potential. For a bee near a
petunia (centre of image), electric field strength becomes much larger
(>5 kV/m) as a positive charge is brought towards a negative charge,
with a good insulator (air) preventing currents from flowing to coun-
ter-act the force. In this modelled scene, both insects and plants influ-
ence the structure and magnitude of the electric field. Electric field is
zero everywhere inside the conductive regions (bees, petunias)
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745J Comp Physiol A (2017) 203:737–748
1 3
extending the flower–bee finite-element model outlined
in the previous section (Fig. 5) to include pollen grains
(Fig. 7).
In the model, we select one of many possible approach
trajectories that could be taken by the bee to the flower
and set a range of parameters for a sum of 2000 pollen
grains. Pollen grains are initially stationary in the model
and located either attached to the flower (where they have
a negative charge of between 0 and −40 fC), or attached
to the ventral side of the bee (where they have a positive
charge of between 0 and +40 fC). All grains had a mass
(m) between 1 and 5 ng. There were three forces included
in the model that influence the motion of individual grains:
gravitational forces (G*m in the downward direction), elec-
tric forces (using Coulomb’s law), and viscous drag (in
low-Reynolds number fluid). Pollen acceleration is mod-
elled as the sum of the forces on the grain divided by the
grain’s mass.
The results of the model show pollen grains of masses up
to and including the mass of maize pollen undergo signifi-
cant electrical forces, with the strong electric field between
flower and bee more influential than gravity (Fig. 7). Pol-
len readily moves against gravitational forces, both from
plant to bee and from bee to plant under the influence of
electrical forces. When we look in detail at the trajectory
of just two pollen grains during the bee–flower interaction,
it is possible to see the contributions of each of these three
forces at successive moments in time (Fig. 7c). For pollen
grain one, at position one (on the bee, t = 0 ms), there is
a repulsive electrostatic force (green arrow) acting on the
positive pollen grain in the direction normal to the sur-
face of the bee (also positively charged). The grain reaches
terminal velocity almost instantaneously as viscous drag
forces in the opposite direction to the velocity of the grain,
quickly balance the other forces. Fifty milliseconds later,
the pollen grain has moved closer to the stigma due to elec-
tric forces and gravity. Here, at point 2, the drag force per-
fectly opposes these other two forces, and the grain moves
at terminal velocity. At this point, the grain is following
a trajectory that would take it below and past the stigma
(points 3 and 4), but as it approaches the stigma, the flo-
ral electric field rapidly increases (Fig. 7b, red zones). This
intensification in the electric field at point 5 (t = 200 ms)
accelerates the grain towards the stigma where it finally
makes contact and is no longer simulated. The second
grain’s journey is similar but in the opposite direction.
Here, the initial force from the plant is again repulsive
(negative pollen and negative plant), followed by attrac-
tive forces from the opposite surface (bee). Gravity plays a
minor role in determining the trajectory of the pollen grains
and simulation with many (2000) grains with varied initial
location, charge or mass shows that almost all, if free to
Fig. 6 Bidirectional pollen
transfer in an electric field.
Daffodil (Narcissus sp.), with
corolla removed was exposed to
the electric field produced by a
triboelectrically charged acrylic
rod, and pollen grain motion
was observed. a Charged rod is
approached to the flower. Pollen
on stigma is highlighted in red,
with close-up of stigma (inset).
b Following the approach of the
charged rod, pollen jumps and
attaches to the rod (red arrow,
inset). c Electrostatically posi-
tively charged rod loaded with
Daffodil pollen, with highlight
of a grain (red outline, inset).
d After approaching the stigma
with a pollen laden rod, the
pollen grain jumps and adheres
to the stigma (inset, red arrow).
In both cases, pollen moves
against gravity force
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746 J Comp Physiol A (2017) 203:737–748
1 3
move, will reach either the protruding sexual organs of the
flower or the hairy surface of the bee (Fig. 7c), as predicted
by Armbruster (2001), Corbet et al. (1982), and Vaknin
et al. (2000, 2001).
This simulation highlights the non-random and organ-
ised directed trajectory of pollen grains under electro-
static forces. Considering the picture generated by both
empirical and modelled data, some questions naturally
arise. Are plants morphologically and physiologically
adapted to increase or take advantage of these electro-
static effects? Do some flower species actively gener-
ate or control the structure and dynamics of the electric
field surrounding them? Are floral electric fields adapted,
much like colours and fragrances are, to signal resource
provisioning to bees, or their readiness for pollination?
Given that bees can perceive detail within the floral elec-
tric field (Clarke et al. 2013), we propose that such adap-
tation is plausible. Electrostatics and electroreception
are likely to be a bona fide part of the multiple co-evo-
lutionary adaptations between plants and their pollina-
tors. For example, Armbruster (2001) suggests that there
is an adaptive compromise at work, where increasing the
length of the stigma also increases the risk of damage to
the structure as it is less well protected by the outer struc-
ture of the flower. Thus, from an electrostatic perspective,
there seems to be clear benefits to pollination for the flat
corolla, tall stigma morphology, though only some flow-
ering plant species have converged on this shape.
Fig. 7 Finite-element modelling and visualisation of bee/flower elec-
trostatic interaction in pollen transfer. a Model construction, showing
the finite-element optimised mesh, and surface charge density (scale
bar, nC/m2). Bee is set up as a positively charged pollen emitter. The
negatively charged flower emitter can be regarded as a stigma or an
anther in this model. b Model solution, showing the electric field
(kV/m) arising between bee and flower, resulting in electric field
hot spots, where electrical forces on charges are higher. The APG
(100 V/m) is included in the model. c Simulation of bidirectional pol-
len grain transfer between flower and bee, taking into account gravi-
tational, electrical, and viscous drag forces. Trajectories of 2000 pol-
len grains between bee and stigma are shown (blue and red lines).
Pollen travelling from the bee to the stigma is positively charged
while pollen originating on the flower and travelling to the bee nega-
tively charged. Pollen charges are uniformly distributed between −40
and +40 fC. Lines show the pollen trajectories and the colour of the
line shows the charge number of the pollen (a dimensionless quantity
equal to the total charge divided by the charge of a proton). Inset is a
closer view of the paths of 25 positively charged pollen grains con-
verging towards the stigma due to its high negative charge density. d
Close-up finite-element visualisation of two pollen grains during their
opposite journey from bee to flower (blue) and flower to bee (red).
Pollen grain colour indicates its charge (red positive, blue negative).
Green arrows show the electric force, cyan the gravitational force,
and magenta the drag force. Black arrows show the total resultant
force. The trajectory for each of the two pollen grains is shown at
50 ms intervals from t = 0 (position 1) to t = 200 ms (position 5).
Force arrows are drawn to scale
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

747J Comp Physiol A (2017) 203:737–748
1 3
Conclusions and future directions
As a recently defined field, there is still a vast amount
that is unknown in the electrical ecology of pollination,
each from the perspectives of the bee the flower and the
electric field. Finite-element models are proving a power-
ful tool in describing electrical interactions between the
bee and the flower, but we need empirical data to con-
firm their predictions under a broader range of condi-
tions. In many cases, the influence of electric fields may
be strongly reduced by environmental factors not simu-
lated in our models. High humidity, for example, leads
to the formation of moist films on surfaces which pre-
vent charge build up, and a dense rainforest canopy acts
like a Faraday cage, negating the influence of the atmos-
pheric electric field at ground level, possibly preventing
the formation of floral electric fields altogether. How do
these different environmental conditions affect the forag-
ing behaviour of pollinators? At the scale of the pollen
grain, even small humidity gradients in the floral head-
space (von Arx et al. 2012) may influence the strength
of electric forces on pollen grains. Does this impact the
efficacy of pollen transfer? Another mitigating factor in
pollen transfer is high winds. It is estimated that wind
forces overpower electrical forces at high wind speeds
(>10 m/s) (Bowker and Crenshaw 2007b), but at lower
speeds, electrical forces are a significant influence on
pollen grain trajectories. Another major direction for
future work should encompass how electrical information
is used to inform animal behaviour. We know that pairing
electrostatic cues with visual cues leads to faster learn-
ing in bumble bees (Clarke et al. 2013). Is this sensory
modality an important part of the “sensory billboard”
advertisement provided by a flower out in a field? Or
could this cue be used to assess the profitability of indi-
vidual flowers? Tarsal hydrocarbon “footprint odours”
left by the previous visitors can indicate resource deple-
tion (Saleh et al. 2007; Wilms and Eltz 2008), could their
“electrostatic footprint” do the same?
The tripartite interactions between bees, flowers, and
the electric field that exist all around them, reveal thus far
underappreciated physical and sensory ecologies. These
interactions are likely to be diverse and maybe ubiquitous
among insects since all are subject to the laws that govern
the force of electromagnetism. The electrical ecology of
bees is not unique. Every flying pollinator of comparable
size to a bee is subject to the same electrostatic forces
from flowers and comparable forces from conspecifics
and other species. Antennae and mechanosensory hairs
are widespread in arthropods (Casas and Dangles 2010)
as is the neural sensitivity required to detect minute
forces on these structures (Yen et al. 1992; Shimozawa
et al. 2003). The tendency to become positively charged
is also not confined to bees. Insect cuticle in general dis-
plays this tendency (Edwards 1962). The generality of
such processes remains to be explored in a wider range
of species and sensory ecological contexts beyond polli-
nation. The ubiquity of electric fields in the environment
means that signals in this modality could potentially be
used by a broad range of species in an array of contexts;
from intraspecific communication to predator avoidance
and prey detection.
Acknowledgements This research and DC and ELM were funded by
grants from the Leverhulme Trust and the BBSRC. The authors wish
to thank G. Sutton and C. Montgomery for their help. DR acknowl-
edges support from the Royal Society London.
Compliance with ethical standards
Conflict of interest The authors declare they have no conflict of inter-
est.
Open Access This article is distributed under the terms of the Crea-
tive Commons Attribution 4.0 International License (http://crea-
tivecommons.org/licenses/by/4.0/), which permits unrestricted use,
distribution, and reproduction in any medium, provided you give
appropriate credit to the original author(s) and the source, provide a
link to the Creative Commons license, and indicate if changes were
made.
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