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Electric Fields Elicit Ballooning in Spiders
Highlights
dSpiders detect electric fields at levels found under natural
atmospheric conditions
dBallooning behavior is triggered by such electric fields
dTrichobothria mechanically respond to such electric fields, as
well as to air flow
dElectric field and air flow stimuli elicit distinct displacements
of trichobothria
Authors
Erica L. Morley, Daniel Robert
Correspondence
erica.morley@bristol.ac.uk
In Brief
Morley and Robert show that spiders can
detect electric fields and respond to this
stimulus by attempting to balloon. They
conclude that atmospheric electrostatics
could provide forces sufficient for
dispersal by ballooning in spiders and
that hair-shaped sensors are putative
electroreceptors.
Morley & Robert, 2018, Current Biology 28, 2324–2330
July 23, 2018 ª2018 The Authors. Published by Elsevier Ltd.
https://doi.org/10.1016/j.cub.2018.05.057
Current Biology
Report
Electric Fields Elicit Ballooning in Spiders
Erica L. Morley
1,2,
*and Daniel Robert
1
1
School of Biological Sciences, Life Sciences Building, University of Bristol, 24 Tyndall Avenue, Bristol BS8 1TQ, UK
2
Lead Contact
*Correspondence: erica.morley@bristol.ac.uk
https://doi.org/10.1016/j.cub.2018.05.057
SUMMARY
When one thinks of airborne organisms, spiders do
not usually come to mind. However, these wingless
arthropods have been found 4 km up in the sky [1],
dispersing hundreds of kilometers [2]. To disperse,
spiders ‘‘balloon,’’ whereby they climb to the top of
a prominence, let out silk, and float away. The pre-
vailing view is that drag forces from light wind allow
spiders to become airborne [3], yet ballooning mech-
anisms are not fully explained by current aerody-
namic models [4, 5]. The global atmospheric electric
circuit and the resulting atmospheric potential
gradient (APG) [6] provide an additional force that
has been proposed to explain ballooning [7]. Here,
we test the hypothesis that electric fields (e-fields)
commensurate with the APG can be detected by
spiders and are sufficient to stimulate ballooning.
We find that the presence of a vertical e-field elicits
ballooning behavior and takeoff in spiders. We
also investigate the mechanical response of putative
sensory receivers in response to both e-field
and air-flow stimuli, showing that spider mechano-
sensory hairs are mechanically activated by weak
e-fields. Altogether, the evidence gathered reveals
an electric driving force that is sufficient for
ballooning. These results also suggest that the
APG, as additional meteorological information, can
reveal the auspicious time to engage in ballooning.
We propose that atmospheric electricity adds key
information to our understanding and predictive
capability of the ecologically important mass migra-
tion patterns of arthropod fauna [8].
RESULTS AND DISCUSSION
In the early 1800s, two competing hypotheses were proposed to
explain how ballooning animals become airborne, invoking (1)
the aerodynamic drag from wind acting on the silk or (2) atmo-
spheric electrostatic forces [9]. Aware of the prevailing argu-
ments, Charles Darwin mused over how thermals might provide
the forces required for ballooning as he watched hundreds of
spiders alight on the Beagle on a calm day out at sea [10].
Darwin’s observation, however, did not provide further evidence
in support of either hypothesis. The physical force required for
ballooning has since been attributed to aerodynamic drag at
low wind speeds (<3 ms
1
)[4, 5, 11], yet the involvement
of electrostatic forces in ballooning has never been tested.
Several issues have emerged when models using aerodynamic
drag alone are employed to explain ballooning dispersal. For
example, many spiders balloon using multiple strands of silk
that splay out in a fan-like shape. Instead of tangling and
meandering in light air currents, each silk strand is kept separate,
pointing to the action of a repelling electrostatic force [12].
Questions also arise as to how spiders are able to rapidly emit
ballooning silk into the air with the low wind speeds observed
in ballooning; the mechanics of silk production requires sufficient
external forces to pull silk from spinnerets during spinning [13].
And, how do low wind speeds provide the high initial accelera-
tions seen in ballooning takeoff [10]? Attempts to find weather
patterns that predict the prevalence of ballooning have been
made, but results remain inconsistent [14]. Mass ballooning
events occur sporadically, and weather conditions on days
with abundant aeronauts cannot be readily distinguished from
days void of them. Although reports claim thermal air currents
and temperature gradients on fair-weather days are the driving
force [15–18], ballooning can be observed when skies are
overcast, as well as in rainy conditions ([14, 15] and E.L.M,
unpublished data). Humidity is potentially an important predictor
[19, 20], but causal and testable explanations are lacking. One
consistent predictor of ballooning is wind speed; spiders only
take flight when wind speed is below 3 ms
1
[11, 15, 17,
19–21], a very light breeze, but models show that these condi-
tions should not allow large spiders to balloon, despite observa-
tion to the contrary [12].
In the early 20
th
century, atmospheric electricity was inten-
sively studied, establishing the ubiquity of the atmospheric po-
tential gradient (APG) [6]; from fair to stormy weather, an APG
is always present, varying in strength and polarity with local
meteorological conditions. Over a flat field on a day with clear
skies, the APG is approximately 120 Vm
1
(Figure S1). In more
unsettled meteorological conditions, charged clouds passing
overhead modify the APG, with rainclouds, storm clouds, and
mist or fog generating APGs of several kilovolts per meter
[6, 22, 23](Figure 1A). Any electrically grounded, geometrically
sharp structure protruding from this flat field will cause a
substantial enhancement of local electric fields (e-fields) [24]
(Figures 1C and 1D). Fundamentally, this is why lightning rods
work to channel a safe, predictable, path for lightning to reach
ground. Because they are rooted in the earth and contain a
high proportion of water and electrolytes, plants tend to equalize
to ground potential [25, 26], and the electric field strength
surrounding leaves and branches, due to their sharp geometry,
can reach many kilovolts per meter [25–27](Figures 1B–1E).
For example, in mildly unsettled weather (APG of 1 kVm
1
), the
2324 Current Biology 28, 2324–2330, July 23, 2018 ª2018 The Authors. Published by Elsevier Ltd.
This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
electric field 10 m above the canopy of a 35-m-tall tree can
exceed 2 kVm
1
(Figures 1B–1E and S1). Closer to the tree,
around sharp leaf, needle, and branch tips, e-fields easily reach
tens of kilovolts per meter (Figures 1B–1E and S1). Local e-fields
can become very high under observed atmospheric conditions;
the potential difference between a grounded plant and the
surrounding air is often high enough to initiate ion emission by
corona discharge [26, 28–31].
APGs and the e-fields surrounding all matter are relevant to
biological systems; for example, bumblebees can detect e-fields
arising between themselves and flowers [27], and honeybees
can use their charge to communicate within the hive [32]. But
beyond bees, how widespread is the ability to detect and use
electrostatic forces in terrestrial organisms? Spider silk has
long been known as an effective electrical insulator; indeed, it
was used in the first quantitative measurements of electrostatic
charge by Michael Faraday and is positioned at the bottom of
the triboelectric series, where it accumulates a net negative
charge [33]. Previous theoretical considerations have proposed
that when silk is charged, the APG can provide sufficient
coulomb force to enable ballooning and aerial suspension using
electrostatic forces alone [7]. Quite surprisingly, APG is rarely
invoked, let alone quantified, in conventional weather descrip-
tors and parameters collected by weather stations. As the APG
plays a role in defining e-fields surrounding vegetation, it is
reasonable to surmise that if e-fields are ecologically relevant,
spiders should be able to detect and respond to an e-field
by changing their behavior to engage in ballooning. Here, we
presented adult Linyphiid spiders (Erigone) with e-fields quanti-
tatively commensurate with atmospheric conditions. Spiders
were placed on a vertical strip of cardboard in the center of a pol-
ycarbonate box, limiting air movement. This box also served as
an APG simulator in the form of a parallel-plate capacitor. This
entire setup was situated within an acoustic isolation and
Faraday cage room (3 m 32.8 m 32.25 m). In their natural envi-
ronment, ballooning spiders take off from protruding branches,
020-20 40-40 60-60
Distance X (m)
0
20
100
40
60
80
Distance Y (m)
Oak tree
Ground
-1
4kVm
D
B
E
C
1
10
2
3
4
5
6
7
8
9
E-field (kV/m)
0
A
0
1
2
3
4
-1
-2
-3
-4
-5
5
03015 2010
525
Time (minutes)
-1
APG (kVm )
0510 15-15 -10 -5
-20 20
6
10
14
18
22
26
30
34
38
Distance X (m)
Distance Y (m)
30 40 50 60
0
2
4
6
8
10
020406080100
Distance Y (m)
10
20
30
40
50
60
70
-1
E-field strength (kVm )
0
1.25
6.25
Figure 1. Quantifying Electric Fields in Nature
(A) Atmospheric potential gradient (APG) measured for 30 min periods across 3 days using a field mill (Chillworth JCI131) at the University of Bristol School of
Veterinary Sciences, Langford. Colors depict recordings from different days in June 2016.
(B) Scale bar for (C) and (D).
(C) Finite element analysis (FEA) model of electric field (e-field) enhancement around a geometrically domed oak tree in an APG strength of 4 kVm
1
.
(D) FEA model detailing the e-field around geometrically sharp tree branches in an APG strength of 4 kVm
1
.
(E) Two-dimensional plot of the e-field along cut lines (red; left inset) of (C) oak modeled as geometrically domed (solid) and (D) branches (dashed) in an APG of
4 kVm
1
(red) and 1 kVm
1
(black). Inset: detail of area indicated by the gray box.
See also Figure S1.
Current Biology 28, 2324–2330, July 23, 2018 2325
leaves, or fences. We used a non-conductive, glue-free card-
board to construct a triboelectrically neutral takeoff site. This
takeoff site generates a spatially uniform and moderate e-field
within the arena (Figure 2A). Vertical e-field strengths across
the arena were either 0 Vm
1
control conditions, 1.25 kVm
1
,
or 6.25 kVm
1
, encompassing APG values observed in over-
cast, misty, and stormy weather [23], as well as e-fields around
grounded trees, grasses, and flowers [6, 25, 30](Figure 1).
There are two behavioral proxies for ballooning in spiders: the
upward extension of the opisthosoma and silk extrusion,
referred to as tiptoeing (Figure 2A), and dropping on a silk drag-
line followed by extrusion of ballooning silk [3]. Although both
behaviors allow spiders to become airborne, tiptoeing exclu-
sively precedes ballooning and is an established predictor of
ballooning propensity [2]. The occurrence of these behaviors
was video recorded under the different experimental treatments
and subsequent analysis scored blind.
Spiders show a significant increase in ballooning in the
presence of e-fields (tiptoes DAIC [Akaike information crite-
rion] between full and null model 42.1, AIC 153.1 versus
195.2, d.f. = 2, p < 10
6
; dragline drops DAIC between
full and null model 28.1, AIC 310.5 versus 282.4, d.f. = 2,
p<10
6
;Figures 2C and 2D). Significantly more dragline
drops are elicited at 1.25 kVm
1
(Z = 2.95; p = 0.003) and
6.25 kVm
1
(Z = 4.87; p < 10
6
), and there is a significant
increase in the number of tiptoes at 6.25 kVm
1
(Z = 4.03;
p<10
6
)(Table S1). The observed change in spider behavior
establishes that they can detect APG-like e-fields. Moreover,
the spider’s unlearned response to e-fields is to engage
in ballooning, and, on becoming airborne, switching the e-field
on and off results in the spider moving upward (on) or down-
ward (off) (Video S1).
The behavioral experiments demonstrate that spiders can
detect e-fields, but what is the sensory basis of spider e-field
Height (cm)
80
60
40
20
01020-10-20 010-10 20
Radial distance from centre (cm)
3
2
1
0
(kV) -1
(kVm )
14
12
10
8
6
4
2
0
20
18
16
5
4
Potential (V) -1
E-field (kVm )
D
Number of tiptoes
0 +1.25 +6.25
2
4
0
***
***
C
Number of dragline drops
0
2
4
6
8
10
12
**
+1.25 +6.25
-1
E-field (kVm ) -1
E-field (kVm )
0
0
AB
1.25
6.25
Figure 2. Spider Ballooning Behavior
(A) A spider showing a typical tiptoe stance.
(B) Finite element model of the electric potential (left) and e-field (right) in the behavioral arena. The electric potential is the potential energy required to move a
charge from one place to another without producing any acceleration: the amount of work per unit charge. It is a scalar quantity. The electric field is a vector
quantity and a force that surrounds an electric charge. It exerts either an attractive or repellin g force on other charges. The base is modeled as ground with 5,000 V
applied to the top plate. A water moat surrounds the takeoff site to prevent spiders escaping over ground. The water was electrically floating, not connected to
ground or a voltage. The scale bar shows electric potential (left) and e-field (right). Aside from small areas around the base of the arena, the e-field is fairly uniform
with a strength of 6.25 kVm
1
(blue color indicated on the scale bar).
(C and D) Boxplots showing the (C) number of dragline drops in response to 1.25 kVm
1
, 6.25 kVm
1
, and zero-voltage control and (D) the number of tiptoes in
response to 1.25 kVm
1
, 6.25 kVm
1
and zero-voltage control (D). Significance levels: ***p < 0.001, **p < 0.01.
See also Video S1 and Table S1.
2326 Current Biology 28, 2324–2330, July 23, 2018
detection? In bumblebees, mechanosensory hairs are the puta-
tive electroreceptors sensitive to e-fields [34]. Arachnids have
mechanosensory hairs known as trichobothria (Figures 3A and
3B). Much is known about their mechanical and neural response
to medium flows (air and water) [35, 36]; they are exquisitely sen-
sitive, detecting air motion close to thermal noise [37], they
detect sound [38], and they are omnidirectional [39]. Early
studies using electrostatic actuation as a tool to investigate
trichobothria mechanics indicate that they may also be sensitive
to e-fields [39–41].
G
Displacement
(nm)
-1
kVm
0
2
-2
013Time (s)
2456789
A
100μm
20μm T
T
MT
MT
Erigone
B
MT
Tb
Time (s)
off
on
Displacement
(μm)
0
5
10
15
20
D
05
10
Time (s)
0
5
10
15
Displacement
(μm)
0 20 40 60 80 100 120 140 160
C
on
off
01020304050
Time (s)
Displacement
(μm)
F
-6
-4
-2
0
2
0
3.6
-3.6
-1
kVm
Displacement
(μm)
0
3.6
-3.6
-1
kVm
0
1
-1
0 50 100 150 200 250
Time (s)
E
01234
Time (s)
Displacement
(nm)
H
40
80
0
2
-2
-1
kVm
-40
0
0
40
-40
80
Figure 3. Mechanical Displacement of Spider Trichobothria
Trichobothria in Erigone.
(A) Diagram of a spider illustrating locations of metatarsal trichobothria and locations for non-contact laser Doppler vibrometry measurement (stars).
(B) Scanning electron microscopy image of adult male Erigone metatarsi and trichobothria, with a close-up view of trichobothrium (inset). Arrows point to the base
of trichobothrium. MT, metatarsus; T, tarsus.
(C–H) Displacement of trichobothria in response to 0.5 ms
1
air flow (C and D), pseudo-DC efield (E and F), and 1 Hz sine e-field (G and H) measured using laser
Doppler vibrometry (LDV). (C), (E), and (G) show single traces, and (D), (F), and (H) show the mean (black) and SD (gray). n = 6 (D), n = 5 (F), and n = 4 (H). Gray
dashed lines indicate the stimulus.
Current Biology 28, 2324–2330, July 23, 2018 2327
We tested the mechanical response of trichobothria on the
front metatarsus to both air flow (0.5 ms
1
) and e-fields using
laser Doppler vibrometry (LDV). Pseudo-direct current (DC) elec-
trical stimuli with 0.1 Hz and 0.01 Hz square waves were used to
simulate a static deflection and rapid change in e-field, as hap-
pens when charged clouds pass overhead (Figure 1). Also, a
1 Hz sine wave was used to investigate the response to slowly
changing e-fields. The response to air flow, a stimulus long estab-
lished to deflect trichobothria, was also measured for compari-
son. Trichobothria are displaced in different ways by DC air
flow and DC e-fields (Figures 3C–3F). In response to air flow, tri-
chobothria are statically displaced for the duration of stimulus
presentation, a tonic response. In contrast, displacement to
e-fields is maximal at the transient switch in voltage, decreasing
back to the baseline over a period of around 30 s, a phasi-tonic
response. Here, the direction of trichobothria displacement is
independent of stimulus polarity; both positive-to-negative and
negative-to-positive stimulus transitions produce displacement
in the same direction, a response indicative of induction charging
where forces are always attractive regardless of stimulus polarity.
Notably, the different types of mechanical response generated
by air movement and e-fields suggest that wind and electric
field detection can be differentiated despite sharing a common
peripheral receptor. The trichobothrium is also displaced in
response to a 1 Hz sine wave (Figures 3G and 3H), showing
that they mechanically respond to slowly varying e-fields, as
well as to rapid changes in potential. Here, the frequency
response of the trichobothrium is twice that of the stimulus (Fig-
ures 4E and 4F); each zero crossing of the stimulus generates a
change in the direction of displacement of the trichobothrium,
providing additional evidence of electrostatic induction. The
response of trichobothria, measured as the number of times the
velocity spikes (Figure 4A), scales linearly with e-field strength
within the range measured (3.6–0.4 kVm
1
). No response above
instrumentation noise (typically 2–10 pm) was elicited from
spines (Figures 4B and 4C). The measurement of tibial spines is
a useful control allowing the exclusion of non-stimulus specific
air motion, electrical crosstalk, or the motion of the entire animal
as potential drivers of the responses measured from tricho-
bothria. Hence, the trichobothria’s mechanical response can be
Time (s)
0102030405060
-1
Velocity (μms )
0
100
-100
-200
-300
2
2
0
-1
kVm
0
100
-200
0102030405060
-100
-300
3.6
-3.6
0
-1
kVm
Time (s)
010
515 20 25 30 35 40 45 50
0
5
10
15
20
Number of spikes
3.6
-3.6
0
-1
kVm
Time (s)
-1
Electric field strength (kVm )
0.4 0.8 1.2 1.6 2.0 2.4 2.8 3.2 3.6
Number of spikes
0
0.2
0.4
0.6
0.8
1.0
C
AB
D
E
Time (s)
01 2 3 456789
10
0
2
-2
-1
kVm -1
Velocity (μms )
20
-20
0
-40
F
-1
Velocity (μms )
0 100 200 300 400
Frequency (Hz)
0
0.4
0.8
1.2
1.2
-1
Velocity (μms )
Figure 4. Velocity of Trichobothria Motion in Response to E-Fields
(A) Transient changes in velocity of a trichobothrium (black, solid line) in response to a 2 kVm
11
e-field oscillating at 0.1 Hz (gray, dashed line).
(B) Transient changes in velocity of a metatarsal spine (black, solid line) in response to a 3.6 kVm
11
e-field oscillating at 0.1 Hz (gray, dashed line).
(C) Spike rate (as seen in A and B) of trichobothria (black; n = 8; ±SD) and metatarsal spine (gray; n = 4; ±SD) across a range of e-field strengths. Spike rate was
measured as the ratio between the total number of zero crossing of the e-field stimulus to the number of spikes coincident (within 25 ms) of stimulus zero
crossings.
(D) Histogram (binned every 25 ms) of the number of velocity spikes of the trichobothria (black; n = 8) and metatarsal spines (white; n = 4) in response to a 0.1 Hz
square wave. The dashed gray line shows stimulus recording.
(E) Velocity of a trichobothrium (black, solid line) in response to an e-field oscillating at 1 Hz (gray, dashed line).
(F) Frequency response (FFT) of trichobothria (black; n = 6; ±SD) in response to a 1 Hz sine wave e-field.
2328 Current Biology 28, 2324–2330, July 23, 2018
considered to result from forces applied to them by the electric
field. Such sensitivity to ambient e-field strength is compatible
with the notion that spider trichobothria can work as electro-
mechanical receptors. The neuroethology of trichobothria in
response to e-fields needs further characterization, to add to
the detailed knowledge of their response to medium flows.
This is the first demonstration of aerial electroreception in
spiders and in arthropods beyond Apidae. The phylogenetic
distance between spiders and bees indicates that aerial electro-
reception could be widespread among the Arthropoda. Conse-
quently, the electromechanical sensitivity of hair structures
present in bumblebees and spiders indicates a possible dual
function, as medium flow sensors and electroreceptors. The
hypothesis thus emerges that the mechanosensory hairs of
many arthropod species may exhibit the additional function of
aerial electroreception.
The present evidence shows that the APG and resulting electro-
static forces are sufficient to elicit ballooning, yet they may not
always be necessary. Aerodynamic drag associated with light
wind and electrostatic forces can work in synergy to facilitate
ballooning. As a result of this work, we propose that the APG
serves at least three functions: an indicator of meteorological con-
ditions, an informational trigger, and a physical driving force
enabling ballooning. Several mechanistic questions now emerge,
pertaining to the dielectric characteristics of ballooning silk and
whether altitude control and navigation take place. Future work
needs to disentangle the complex interplay between animal
behaviorand variations in the APG. Inclusion of the APG as a mete-
orological parameter has the potential to provide better predic-
tions of dispersalevents and the distribution of spiderpopulations.
Understanding the mechanisms that underpin dispersal is
crucial for describing biomass and gene flow, population dy-
namics, species distributions, and ecological resilience to sto-
chastic changes. It is therefore of great importance for global
ecology. Spiders are a powerful source of biological control,
consuming 400–800 million tons of biomass globally each year
[42], significantly impacting the composition and diversity of
ecosystems [43]. The terrestrial biological world has evolved
within the APG and the use of e-fields in dispersal could extend
beyond ballooning spiders to those species of caterpillar
(Lepidoptera) and spider mite (Trombidiformes) that also
disperse aerially [2], as well as plant propagules. As ballooning
arthropods constitute a proportion of significant seasonal bio-
flows [8], studying the role of atmospheric electricity and its
detection by arthropods has implications for predicting the
transport of nutrients, pathogens, agricultural pests [44–46],
and their predators between ecosystems and biomes [8].
STAR+METHODS
Detailed methods are provided in the online version of this paper
and include the following:
dKEY RESOURCES TABLE
dCONTACT FOR REAGENT AND RESOURCE SHARING
dEXPERIMENTAL MODEL AND SUBJECT DETAILS
dMETHOD DETAILS
BBehavioral experiment set up
BProtocol for behavioral experiments
BTrichobothria mechanics
BElectric field models
dQUANTIFICATION AND STATISTICAL ANALYSIS
dDATA AND SOFTWARE AVAILABILITY
SUPPLEMENTAL INFORMATION
Supplemental Information includesone figure, one table, and one video and can
be found with this article online at https://doi.org/10.1016/j.cub.2018.05.057.
A video abstract is available at https://doi.org/10.1016/j.cub.2018.05.
057#mmc4.
ACKNOWLEDGMENTS
E.L.M. would like to thank Andrew Mason for encouraging the collection of pi-
lot data. Both E.L.M. and D.R. thank four anonymous reviewers for construc-
tive comments that allowed improvement to our manuscript. E.L.M. and D.R.
were supported by grants from the UK BBSRC (BB/M011143/1) and European
Research Commission (ERC ADG 743093).
AUTHOR CONTRIBUTIONS
Conceptualization, E.L.M.; Methodology, E.L.M. and D.R.; Investigation,
E.L.M; Writing – Original Draft, E.L.M.; Writing – Review & Editing, E.L.M.
and D.R.; Resources, D.R.
DECLARATION OF INTERESTS
The authors declare no competing interests.
Received: September 19, 2017
Revised: May 4, 2018
Accepted: May 18, 2018
Published: July 5, 2018
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2330 Current Biology 28, 2324–2330, July 23, 2018
STAR+METHODS
KEY RESOURCES TABLE
CONTACT FOR REAGENT AND RESOURCE SHARING
Further information and requests for resources and reagents should be directed to and will be fulfilled by the Lead Contact, Erica
Morley (erica.morley@bristol.ac.uk).
EXPERIMENTAL MODEL AND SUBJECT DETAILS
Erigone spp. were caught by balloon trap [49] at the University of Bristol School of Veterinary Sciences, Langford between July and
October 2016. They were housed individually at 17C on 12:12 hr light dark cycles until the start of experiments. Adult males and
females were identified by examining palps and epigyne under a light microscope.
METHOD DETAILS
Behavioral experiment set up
Behavioral responses of adult Erigone to different electric field strengths were observed under experimental treatments with a
repeated-measures, randomized block design. The experimental arena comprised a polycarbonate box (0.9 m 30.9 m 30.9 m)
to limit air motion, with a door on one side for access. An aluminum plate (0.8 m 30.8 m) was attached inside the top of the box
and an identical aluminum plate was positioned on the bottom of the box to give a plate separation of 0.8 m. The plates were con-
nected to a high voltage power supply (PS350; Stanford Research Systems, Sunnyvale, CA, USA), with one plate electrically
grounded and the other connected to either 0 V, 1000 V or 5000 V to give electric field strengths of 0 Vm
1
, 1.25 kVm
1
or
6.25 kVm
1
respectively. A plastic dish (37 cm diameter) with a glue-free cardboard strip oriented vertically (25 cm, 1 m at the
base tapering to 2 mm at the tip) was positioned in the center of the box. The takeoff site was surrounded by shallow water to limit
the escape of spiders. The water was not connected to ground or voltage and was electrically floating. The entire setup was situated
on an anti-vibration table (Newport RS4000; Irvine, CA, USA) within an acoustic isolation and Faraday cage room (2.8 m 33m3
2.25 m). Temperature and humidity levels were monitored throughout experiments (21.2± 0.9; 50.5% RH ± 5.4).
Spider behavior was subsequently assessed by video analysis. To minimize experimenter bias, videos were scored blind. The
number of tiptoe events and dragline drops were recorded during the 2-min treatment. Tiptoes were defined as holding the typical
tiptoe stance (Figure 2A) for at least 3 s. Attempts that did not meet this criterion were not counted.
Protocol for behavioral experiments
In each trial, spiders were placed individually at the top of the takeoff site. They were given an initial 5 min settling period, following
which the treatment was turned on and their behavior filmed (Canon EOS 700D, Canon Macro EF 100 mm 1:2.8 L IS USM; Canon,
Tokyo, Japan) for 2 min. After 2 min, the treatment was switched off and the filming stopped. The spider was then removed and put
back in its vial. Each spider was subjected to 3 treatments in a randomized order. Only 1 treatment was tested per animal each day
and trials were completed across consecutive days. Between each trial the takeoff site was wiped with a cloth containing 70%
ethanol and allowed to dry to remove silk and possible chemical cues left by the spider in the previous trial. Any residual charge
was neutralised between each trial using an anti-static gun (Zerostat 3; Milty), and monitored using a custom built electroscope.
The effect of electric field strength was tested using positive voltages applied to the top plate (1000 V, 5000 V) and a control (0 V).
REAGENT or RESOURCE SOURCE IDENTIFIER
Deposited Data
Experimental data and COMSOL models This paper https://doi.org/10.17632/8vpyymcrt4.1
Experimental Models: Organisms/Strains
Erigone spp. Langford School of Veterinary Sciences, Bristol, UK N/A
Software and Algorithms
COMSOL Multiphysics 5.3a COMSOL Multiphysics https://www.comsol.com/
MATLAB 2014a Mathworks https://www.mathworks.com
R Studio version 0.99.893 [47]https://www.rstudio.com/
lme4 package for R [48]https://cran.r-project.org/web/packages/
lme4/index.html
PSV version 9.0 Polytec https://www.polytec.com/eu/
Current Biology 28, 2324–2330.e1–e2, July 23, 2018 e1
The voltage was applied to the top plate with an electrically grounded bottom plate. To control for experimenter disturbance, the 0 V
control treatment was carried out in the same way as the voltage treatments; the power supply was physically disconnected from the
behavioral set up before the trial began, and the power supply was manually switched on and off in the same way as the voltage
treatments to cause the same level of disturbance as in other treatments, but without any applied voltage.
Trichobothria mechanics
The mechanical response of trichobothria to electrostatic fields was measured in adult male Erigone using laser Doppler vibrometry
(LDV) (Polytec PSV 400, Polytec, Waldbronn, Germany). Spiders were anaesthetised using CO
2
and affixed by the dorsal prosoma
to a wooden stick (tip diameter 1mm) using liquid latex. The opisthosoma, legs and palps were all immobilised using liquid latex and
the spider was positioned so that the metatarsal trichobothrium on one of the first pair of legs was within focus of the laser beam and
coaxial camera, using a close-up attachment (PSV-A-410; Polytec, Waldbronn, Germany). Parallel aluminum plates (15 cm 311 cm)
were positioned above and below the spider, 10cm apart. The top plate was connected to a voltage source (Agilent 33120A; custom
built high voltage amplifier) and the bottom plate was electrically grounded. The entire set up was placed on an anti-vibration table
(TMC 784-443-12R; Technical Manufacturing, Peabody, MA, USA) within an anechoic chamber (2.25 m 32.7 m 32.6 m) electrically
isolated by Faraday caging.
The pseudo-DC voltage comprised a square wave of 0.01 Hz at 360 V peak-to-peak (pp) (3.6 kVm
1
), to allow for a clear displace-
ment measurement. The velocity of trichobothria response to a 0.1 Hz square wave in voltages steps from 360 V (3.6 kVm
1
)to40V
(0.4 kVm
1
) was also measured, along with the displacement and velocity response to a 1 Hz sine wave at 200 V (2 kVm
1
).
Measurements were made in the time domain, digitized via an on-board data acquisition card (National Instruments PCI- 6110)
and subsequently analyzed by using PSV software (Polytec version 9.0). Data analysis was carried out in MATLAB 2014a
(Mathworks, Natick, MA, USA).
Electric field models
Finite element models of the APG around trees and e-fields within the experimental arena were generated using COMSOL Multi-
physics (COMSOL 5.3a, Stockholm, Sweden). The models of the APG-tree interactions were produced by modeling the APG during
unsettled weather with an electric field strength of either 1 kVm
1
or 4 kVm
1
. Here, electrical ground was beneath 5 m of soil which
had an electrical boundary with the tree. The electric potential was modeled as a plate above the air. To model the experimental arena
a cardboard takeoff site (with appropriate material properties) was generated inside a volume of air of the same dimension as the
arena. Below the takeoff site a dish of water was modeled. The bottom surface was held at ground potential while the top plate of
the arena was set at 5000 V, the maximum used in behavioral experiments. The cardboard blade and water dish were left electrically
floating, as they were in the arena itself.
QUANTIFICATION AND STATISTICAL ANALYSIS
The ballooning behavior data was analyzed using generalized linear mixed models (GLMM) using the lme4 [48] package in R Studio
version 0.99.893 [47]. All data was in the form of counts and a total of 36 animals (n = 36, 20 males and 16 females) were used in the
behavioral study. Each animal was subjected to all e-field treatments (0 V/m, 1.25 V/m and 6.25 V/m), therefore the analysis needed to
include spider identification as a factor to incorporate the repeated-measures design into the statistical analysis. Data was bounded
at 0 (count data) and due to singularity, models with different intercepts and slopes did not converge, a simple random effects model
was therefore used with a common slope but different intercepts. To test for the effect of voltage treatment on behavior a full model
was compared to a null model with treatment removed using ANOVA and DAIC scores. The random factor in each test was the
individual spider (1jspider identification) while the fixed factor was the voltage treatments tested. Tests used Poisson error and a
log link function. Median and interquartile ranges for the data are shown in Figure 2 along with significance values and GLMM outputs
are described in Table S1.
DATA AND SOFTWARE AVAILABILITY
Experimental data and COMSOL models are made available through Mendeley Data and can be accessed at https://doi.org/10.
17632/8vpyymcrt4.1.
e2 Current Biology 28, 2324–2330.e1–e2, July 23, 2018
