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First published online November 14, 2008
Journal of Experimental Biology 211, 3682-3690 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.019901
Static electric field detection and behavioural avoidance in cockroaches
1 School of Biological Sciences, Biomedical Science Building, University of
Southampton, Bassett Crescent East, Southampton SO16 7PX, UK
2 School of Engineering Sciences, University of Southampton, Southampton SO17
1BJ, UK
3 Animal Behavior and Intelligence, Division of Biological Sciences, Graduate
School of Science, Hokkaido University, Sapporo 060-0810, Japan
* Author for correspondence (e-mail: pln{at}soton.ac.uk)
Accepted 23 September 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: electric fields, high voltage, sensory, mechanoreception, behaviour, cockroach
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Heiligenberg and Bastian,
1984; Kalmijn,
1988). The nematode, Caenorhabditis elegans, orientates
to electric fields, which appear to activate amphid sensory neurones
(Gabel et al., 2007) whereas
electrostatic forces from frictionally charged surfaces alter insect
locomotory behaviour (Edwards,
1960b; Maw, 1961;
Maw, 1962;
Watson et al., 1997).
Changes in an insect's behaviour occur in response to a variety of electric
field types, including charged surfaces, static or fluctuating electric fields
generated by high voltage power supplies and very low frequency (VLF) electric
fields produced by high voltage power lines. Insects respond to charged
surfaces by avoiding, or being repelled by, the charged region
(Hunt et al., 2005;
Maw, 1964). The movements of
parasitoids decrease when walking across charged surfaces
(Maw, 1961), suggesting that
such surfaces could be exploited as a non-toxic pest control method
(Jackson and McGonigle, 2005;
Maw, 1962;
McGonigle et al., 2002).
Electric fields of strengths that occur under high voltage power cables
have led to studies of the possible adverse effects of electric fields on
insects, including chromosome aberrations and paralysis
(McCann et al., 1993;
McCann et al., 1998;
Watson, 1984), and changes in
locomotion and movement (Edwards,
1960a; Edwards,
1961; Perumpral et al.,
1978). However, despite these reports, there have been few
systematic analyses of the behavioural responses of insects to static and VLF
electric fields. Little is known, for example, of the interactions between an
insect's body and the electrical forces acting on it, and how electric fields
are actually detected. Insect appendages are thought to be influenced by both
static and VLF electric fields. For example, the wings of Drosophila
and bees vibrate when exposed to both static and VLF electric fields
(Bindokas et al., 1988;
Watson et al., 1997) whereas
the antennae of bees and parasitoids appear to be deflected by electric fields
(Maw, 1961;
Yes'Kov and Sapozhnikov,
1976). It is possible, therefore, that insect appendages are
involved in the detection of electric fields, much in the same way that body
hairs are believed to contribute to the perception of electric fields by
humans (Chapman et al., 2005).
Body hairs are deflected by electric fields with the angle of displacement
being proportional to the field strength
(Shimizu and Shimizu, 2003;
Shimizu and Shimizu, 2004) and
removal of hairs abolishes our ability to detect such fields
(Chapman et al., 2005).
In the present study we have systematically analysed cockroach behaviour in response to static electric fields and utilising a number of different approaches we have asked if insects have an electrosensory sense, how they detect static electric fields and how that information is used to drive adaptive behaviour.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Y-tube behavioural bioassay
Three cylindrical, 2 mm thick, silicon glass chambers, 150x30 mm
(lengthxdiameter), were fused together in a `Y' configuration 120 deg.
apart (Fig. 1A). A small hole
(7 mm diameter) was cut out of the upper surface near the entrance to each
anterior chamber into which a copper loop electrode, 5x28 mm
(widthxdiameter), was fixed. Aluminium earth bands were fixed 35 mm from
the end of each chamber and a high voltage power supply (Brandendurg Alpha
III, Brandenburg, UK) supplied the electrodes. Two capture chambers
(85x35 mm) (lengthxdiameter) covered the ends of each anterior
chamber to catch the cockroach after every trial, and a release chamber
(85x35 mm) (lengthxdiameter) was placed at the base of the Y-tube.
The power supply was adjusted to produce electric fields at applied potentials
of 0 V, 0.5 kV, 0.75 kV, 1 kV, 2 kV, 3 kV or 4 kV in one pathway, before a
cockroach entered the central chamber and the pathway taken by the cockroach
determined. Control trials without electric fields were carried out to test
for natural preferences within the Y-tube. Cockroaches that spent longer than
5 min in the apparatus, or returned back down the central chamber, were
discounted from the analyses. The decision time was defined as the time taken
for an animal to pass from the release chamber to a position of one body
length past an electrode. Statistical analyses were carried out using a
Bionomial Tests of Proportions (S-Plus, v. 6.1 for Windows) and
2 tests.
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Electric field stimulation of antennae
To investigate the effect of static electric fields on antennal deflection,
the head of an adult cockroach (N=5) was positioned 50 mm from a
circular copper electrode (30 mm diameterx7 mm width) after
anaesthetisation with CO2 and restrained in PlasticineTM.
Another electrode was positioned at the posterior of the cockroach and
connected to earth whereas the anterior electrode was connected to the high
voltage power supply. Antennal deflection was analysed at stimulus outputs of
3 kV, 4 kV, 5 kV and 6 kV with five trials of 5 s exposure for each individual
with 15 s between each trial. All trials were recorded using a digital camera
(Sanyo VCB-3372P, Tokyo, Japan) onto DVD (Panasonic DMR-E55EB, Osaka, Japan)
for subsequent analysis.
Magnetic field stimulation of antennae
Preliminary studies showed that the application of fine iron powder
(spherical, <10µm diameter, Alpha Aesar, Karlstruhe, Germany) to the
antennae was sufficient to deflect the antennae under magnetic fields.
Cockroaches exposed to magnetic fields were positioned opposite an
electromagnet at the same height and distance to the source as individuals
tested under electric fields. After anaesthetisation the distal two-thirds of
one antenna was coated in a pre-weighed quantity of iron powder
(0.0153±4x10–4 g, N=5) using a fine
paintbrush and any excess gently removed. The effects of four magnetic field
strengths on antennal deflection were investigated. It was not possible to
measure the magnetic field strengths within the chamber and, thus, the
displacements caused by magnetic stimulation were therefore calibrated against
displacements caused by electric fields at electromagnet potentials of 20V,
25V, 30V and 35V (Nihon-Kohden SEN-3301) (see
Fig. 2 and
Fig. 3C). Control experiments
were also carried out to determine if magnetic fields affected the movement of
antennae not coated with iron particles. The antennae of each individual was
deflected five times (5 s duration) at each electromagnetic coil voltage with
15 s between trials. All experiments were recorded (Sony DCR-TRV9) and video
digitised (Apple PowerBook G5, CA, USA) for further analysis.
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Differences in mean antennal deflection between field types were analysed using Student's t-tests (SPSS for Windows, v. 14, Chicago, IL, USA) after assumptions of normal distributions and homogeneity of variances were met. Regression analysis was carried out to test for the effect of potential on antennal deflection for each field type (Minitab for Windows, v. 12, PA, USA). A Student's t-test was also performed to compare regression coefficients and highlight any differences in the effect of voltage potential on antennal deflection between the field types.
Physiological recording
The interneurons that receive input from mechanosensory neurones from the
antennae are bundled within the interganglionic neck connective region of the
VNC (Burdohan and Comer, 1996)
and have axons on the side contralateral to their input side. These
interneurones were recorded extracellularly from their axons between the
subesophageal ganglion and the prothoracic ganglion
(Burdohan and Comer, 1996;
Comer et al., 2003). To expose
the neck connectives, a small incision was made along the ventral edge of the
neck and the remaining soft cuticle removed with fine iridectomy scissors. The
connective contralateral to the antenna to be deflected was isolated from
surrounding muscle and tissue and placed on a bipolar hook electrode (125
µm silver, Teflon® coated except at the tips), insulated with petroleum
jelly and the signals amplified and stored on a computer.
Action potentials, spikes, were amplified (Nihon Kohden MEG-1100), displayed on an oscilloscope (Tektronix 5111A, Beaverton, OR, USA) and digitally recorded using a PowerLab digital acquisition system (ADInstruments, Colorado Springs, CO, USA) running Chart v. 4.01 software. Spike threshold levels were determined using Chart software and the number of large amplitude spikes were compared in a time window 320 ms before stimulus onset (control) with one 320 ms after stimulus onset (test).
Ablation of sensory structures
Mechanoreceptor activation was prevented at various regions of the antennae
(the scape, pedicel or flagellum) of third- and fourth-instar cockroaches
(abdomen to head length, N=263, 8.06±0.56 mm) to determine
which mechanoreceptors contribute to the detection and avoidance of electric
fields. This was done by applying a non-toxic cyanoacrylate adhesive,
VetBond® (WPI, Stevenage, UK), to parts of the head and antennae to
prevent movement about specific joints of the antennae using a fine
microcapillary held in a micropipette holder. Adhesion was subsequently aided
by applying cyanoacrylate adhesive accelerator (RS Components, Corby, UK).
This procedure was carried out on the head capsule–scape joint and the
scape–pedicel joint. Ablation of the flagellae was carried out using a
pair of fine iridectomy scissors after anaesthetising and restricting the
movements of animals, which were then allowed to recover for 18–20 h
before testing. Exteroceptive input from hair plate hairs was prevented by
applying cyanoacrylate adhesive to the hair plates only. The effect of field
strength on avoidance behaviour was analysed using 2 tests of
association for each type of antennal sensory input modification carried
out.
High-speed video observation of antennae
The influence of electric fields on cockroach antennae approaching the
copper electrodes was filmed in the horizontal plane through the Y-tube
apparatus using high-speed video equipment (MotionScope 1000S, Redlake
Imaging, CA, USA). Video images were taken of cockroaches, at 250 frames
s–1 (N=4), exposed to electric fields at 1 kV and 4
kV potentials, in addition to controls.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The behaviour of cockroaches was first analysed within an untreated Y-tube apparatus to determine if a natural bias for one pathway existed, however, no natural preference for either the left or right untreated pathway was exhibited (N=40, P>0.05) (Fig. 1C,F). The effects of electric field strength on cockroach avoidance were then tested at applied voltage potentials of 0.5 kV, 0.75 kV, 1 kV, 2 kV, 3 kV and 4 kV and the preference of cockroaches for the treated or untreated pathway determined. Potentials applied at 0.5 kV and 0.75 kV caused no clear effects on the walking behaviour of cockroaches nor any significant preference for cockroaches to take either the treated or untreated pathway (Fig. 1E) (N=40, P>0.05 for both cases, Mann–Whitney U-test). Increasing the voltage to 1 kV and above resulted in cockroaches spending significantly more time in the decision zone around the intersection of the tubes, as their walking speed declined on approaching a field and a different path eventually taken (Fig. 1E). Moreover, a significantly greater number of animals avoided the treated pathway of the Y-tube (N=40, P<0.01, Mann–Whitney U-test) (Fig. 1F). A preference for the untreated (not charged) pathway continued to be exhibited when the electrode was charged at 2 kV, 3 kV and 4 kV (N=40, P<0.01 in all cases, Mann–Whitney U-test) (Fig. 1F).
Thus, cockroaches exhibit a clear avoidance of electric fields at applied electrode voltages over 1 kV, equivalent to a modelled electric field strength of 8–10 kV m–1.
The antennae are responsible for the detection of static electric fields
Previous studies have shown that activation of mechanoreceptors on and in
the antennae mediate escape behaviour and avoidance in response to predator
attack or tactile stimulation (Comer et
al., 2003; Ye and Comer,
1996). Given previous reports of electric fields influencing
insect antennae (Maw, 1961;
Yes'Kov and Sapozhnikov,
1976), we investigated whether static electrical fields could
cause antennal movement, thereby activating mechanoreceptors that could in
turn elicit avoidance behaviour.
Single frames from high-speed video showed the influence of static electric fields on cockroach antennal deflection within the Y-tube apparatus. While the antennae of cockroaches within an untreated pathway were not affected when the copper electrode was approached (Fig. 2A) (N=4), applying a 1 kV potential resulted in a clear attraction of the flagellae towards the electrode (Fig. 2B) (N=4) (Fig. 3C,D).
To determine what sensory receptors (Fig. 2C) might be activated by this deflection and could, in turn, contribute to avoidance, the effect of preventing specific antennal sensory inputs on the behaviour of freely moving cockroaches was analysed. Experiments were first carried out to control for any effect of preventing antennal mechanoreceptor input on natural preference within the Y-tube apparatus (Fig. 2D). Restricting antennal movement or ablating the antennae did not result in a significant preference for the left or right pathway (N=40, P>0.05 in all cases) in the absence of an electric field. In addition, sham experiments demonstrated that VetBond® application had no effect on preference behaviour (N=40, P>0.05).
When a 1 kV potential was applied to the electrode of one arm of the Y-tube, over 80% of intact animals avoided the electric field (Fig. 2E). Preventing all antennal sensory input by ablating the antennae resulted in animals showing no significant preference for the treated or untreated pathways. Preventing the activation of mechanoreceptors on the scape and pedicel by covering the head–scape and scape–pedicel joints with glue also caused significantly less avoidance than in intact control cockroaches (N=40 P<0.05). Preventing movement of the antennae about the head–scape joint alone resulted in significantly less avoidance than intact control cockroaches (N=40, P<0.05) whereas fixing the scape–pedicel joint alone had no significant effect on avoidance compared with control animals, with 80% of individuals avoiding the charged arm of the Y-tube (N=39, P>0.05). Finally, applying glue directly to the hair plates on the scape and pedicel, while still allowing joint movement, also significantly reduced avoidance (N=47, P<0.05). These results suggest that mechanoreceptive hair plates at the base of the scape are important in detecting movements of the antennae caused by electric fields and contributing to avoidance behaviour.
Using magnetic fields to deflect the antennae
To determine whether antennal deflection caused by electric fields evoked
changes in neural activity that could underlie the detection of electric
fields, it was necessary to develop an alternative method to deflect the
antennae without the use of electric fields that prevent electrophysiological
analysis due to electrical `noise'. We, therefore, developed a method
combining magnetic field stimulation with the application of fine iron powder
to the antennae to mimic the movements of the antennae caused by electric
fields. Without iron powder, magnetic fields of varying strength did not have
an effect on antennal movement (F1,15=2.29,
P>0.05), demonstrating that magnetic fields per se did
not influence the movement of antennae without iron powder
(Fig. 3A). Following coating of
the antennae with iron powder, magnetic fields deflected the antennae toward
the coil tip (Fig. 3B).
Similar antennal deflections were generated for both field types (electric or magnetic) at four potential pairings. For a given pairing, antennal deflection did not differ between field types (Fig. 3B) (N=5, P>0.05 in all cases), demonstrating that the electrical and magnetic forces acting on the antennae at each pairing had similar effects on the antennae. Antennal deflection caused by a 20 V magnetic coil potential was therefore analogous to a deflection elicited by a 3 kV electric potential; deflection due to a 25 V magnetic coil potential was the same as a 4 kV electric potential; deflection by a 30 V magnetic coil potentials similar to a 5 kV electric potential; and 35 V was the same as 6 kV.
Increasing the magnetic or electric field strength by increasing the potential had a proportional effect on antennal deflection. Regression analysis showed that as the magnetic potential was increased the antennal deflection became significantly greater (b=0.84, t=2.55, P<0.05) (Fig. 3D). There was no significant difference between the regression slopes of antennal deflection caused by magnetic and electric fields as the voltage potential was altered (t=0.35, d.f.=1, P>0.05).
Antennal displacement evokes interneurone activity in VNC
Extracellular recordings of neural activity were made from the VNC to
investigate whether deflection of the antennae led to elevated levels of
activity in intersegmental interneurones in the VNC. Control experiments using
antennae not coated with iron particles showed that exposure to magnetic
fields was not associated with changes in antennal deflection and VNC activity
when magnetic potentials were applied (N=5, t=0.18,
P<0.05), indicating that magnetic fields per se did not
influence neural activity (Fig.
4A,Ai). Deflecting a coated antenna with a magnetic field resulted
in a significant increase in VNC activity (N=5, t=3.4,
P<0.05) and a significant deflection of the antennae
(Fig. 4B,Bi).
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Behavioural responses to magnetic fields
To confirm that antennal deflection caused by magnetic fields in fixed
animals could affect the ability of cockroaches to avoid magnetic fields
during free movement, we placed individuals with antennae coated with iron
particles in a Y-tube apparatus combined with electromagnets
(Fig. 6A). Control trials with
no magnetic fields showed that cockroaches with coated antennae exhibited no
side preference (N=32, P>0.05). However, cockroaches did
not appear to significantly avoid magnetic fields (N=27,
P>0.05). This was most likely due to the antennae on insects with
iron particles sticking to the magnets and thereby completely abolishing
normal avoidance patterns. However, as with electric field avoidance
(Fig. 1C), individuals took
significantly longer to make a decision when approaching the magnetic field
than when no magnetic fields were present
(Fig. 6B) (N=44,
P<0.01). Moreover, control studies showed that magnetic fields
alone did not have an effect on behaviour as there was no significant
difference in the decision time taken by cockroaches in the Y-tube
(Fig. 6B) (N=40,
P>0.05).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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).
Cockroaches actively avoided the charged arm of a choice chamber indicating
that electric fields can be detected and the information used to generate
avoidance responses. These findings support previous observations, for example
Watson (Watson, 1984), who
showed that Drosophila movement is also correlated with field
strength. Our results suggest that cockroaches exhibited a `threshold' of
avoidance at static electric field strengths of 8–10 kV
m–1. Atmospheric electric fields have been reported to cause
behavioural changes in insects (Edwards,
1960a; Maw, 1962)
and static electric fields up to 20 kV m–1 can be generated
by equipment such as televisions. Underneath high voltage power lines, static
electric fields can reach 11 kV m–1 at ground level and far
higher at closer proximity to the power line
(Fews et al., 1999a;
Fews et al., 1999b). The
results of the present study showed that avoidance and behavioural changes
occurred in free-moving cockroaches confronted with static electric fields of
8 kV m–1 and above. Therefore, this finding implies that
static electric fields from household and office equipment could cause changes
in insect behaviour. In addition, our results may explain previous
observations that suggest that the flying activity of insects is altered near
high voltage power lines (Orlov,
1990; Orlov and Babenko,
1987).
The detection of static electric fields
Some animals have evolved specialised means of detecting forces such as the
Earth's magnetic and electric fields. For example, magnetite
(Fe3O4) is deposited in specific regions of certain
insects and birds, allowing them to detect magnetic fields
(Maher, 1998;
Wiltschko and Wiltschko,
2006). Likewise, some aquatic animals can perceive the Earth's
magnetic field using specific structures, such as the ampullary organs
(Kalmijn, 1971;
Kalmijn, 1982). The ampullary
organs are also used to generate and detect weak electric fields within sea-
and freshwater; an ability that is utilised during prey localization,
communication and navigation (Heiligenberg
and Bastian, 1984; Hopkins,
1988; Kalmijn,
1988).
Given the evolution of specific structures to detect the many external cues
in the environment, a key focus of the present study was to determine whether
insects have also evolved specific sensory structures to detect electric
fields. We found through ablation studies that the antennae were crucial for
the detection of electric fields and without them a cockroach is not able to
avoid a static electric field. Further fixation studies revealed that hair
plates at the base of the scape (S-HPs) were crucially required for an animal
to avoid an electric field. The influences of electric fields on other
slender, elongated structures, such as human hairs have previously been
reported (Chapman et al., 2005;
Shimizu and Shimizu, 2003;
Shimizu and Shimizu, 2004).
Our results show that the detection of static electric fields by cockroaches
can be attributed to the activation of an established sensory system and not
one that has evolved specifically for the purpose.
Cockroaches approaching a static electric field are subject to considerable
electrical forces, clearly illustrated by the antennal deflection observed
through high-speed video caused by attraction forces pulling the antennae to
the electrode. Before encountering an electric field, the charges on a
cockroach are randomly distributed (Fig.
7A). When approaching a positively charged electrode, as used in
our experiments, this induces an uneven charge distribution on the cockroach
with negative charges attracted towards the electrode and, hence, leading to a
passive bending of the antennae towards the electrode by the attraction of
opposite charges (Fig. 7B). The
imposed deflection of the antennae is detected by sensory receptors leading to
a marked bending of the antennae as they are actively withdrawn from the
forces attracting them to the electrode. Thus, the cockroaches use their
antennae as multi-modal sensors to detect many external cues
(Bell and Adiyodi, 1981).
Electric fields cause displacement of the antennae about the head–scape
joint, deflecting S-HP sensilla. There are three S-HPs on adult cockroach
antennae located on the dorsal, medial and lateral surfaces
(Staudacher et al., 2005) that
detect antennal position in all planes
(Okada and Toh, 2001). We have
clearly established that it is the displacement of the antennae by electrical
forces that are detected by the S-HP mechanoreceptors, enabling an animal to
perceive static electric fields. The antennae are known to play a crucial role
in insect behaviour and their deflection evokes avoidance or escape movements
(Camhi and Johnson, 1999;
Comer et al., 2003;
Cowan et al., 2006;
Okada and Toh, 2006).
Information on antennal position is not only provided by the hair plates on
the scape but also from pedicel hair plates, from the flagella and from
internal movement detectors (Comer et al.,
2003; Okada and Toh,
2000; Okada and Toh,
2006; Staudacher et al.,
2005). Together, they provide information about deflection of the
antennae in all planes of movement (Okada
and Toh, 2001; Staudacher et
al., 2005).
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; Comer et
al., 2003; Cowan et al.,
2006; Okada and Toh,
2006). Hence, displacement of the antennae by electric fields
activates sensory receptors involved in generating avoidance responses. The
scape hair plates mediate a variety of behaviours, not only in cockroaches but
also in a number of insects including locusts
(Gewecke, 1974), stick insects
(Durr et al., 2001), bees
(Kloppenburg, 1995) and
crickets (Staudacher et al.,
2005). Such behaviours include locomotion and flight, antennal
avoidance reflexes and object orientation
(Gewecke, 1974;
Okada and Toh, 2000;
Sherman and Dickinson, 2004;
Staudacher et al., 2005).
Notably, the basal joints play an important role in triggering cockroach
escape away from the direction of an antennal stimulus
(Comer et al., 1994;
Ye et al., 2003). Together,
the influences of electric fields on antennae and the behaviour mediated by
scape hair plates may therefore underpin the avoidance evoked by cockroaches
confronted with static electric fields.
Descending interneurones and the avoidance of static electric fields
To demonstrate that antennal deflection caused by electrical forces could
lead to changes in the activity of interneurones involved in avoidance
responses, we developed a method of deflecting the antennae using magnetic
fields to mimic the deflections caused by electric fields. These experiments
showed that the magnetic fields themselves did not cause a change in behaviour
of the insects but that when combined with deflection of the antennae covered
in iron powder they did.
Stimulation of the antennae has a substantial effect on thoracic motor
output, believed to be controlled by connections between descending
mechanosensory interneurones (DMIs) and thoracic interneurones (TIs)
(Ritzmann and Pollack, 1994;
Ritzmann and Pollack, 1998).
We showed that the activity of the VNCs, which is likely to result from DMIs
activation (Burdohan and Comer,
1996; Ye and Comer,
1996), increased when the antennae were deflected using magnetic
stimulation, suggesting that the DMIs responded to antennal deflection.
Previous studies have shown that the DMIs converge onto TIs and cause TI
excitation and, subsequently, movement
(Ritzmann et al., 1991). Given
the similarities in the influences of magnetic and electric fields on
cockroach antennae, our results suggest that the DMIs are, at the very least,
partly involved in mediating the avoidance of static electric fields.
Mechanosensory afferents from both the head–scape and
scape–pedicel joints project primarily to the deutocerebrum via
the antennal lobe (Okada and Toh,
2000; Staudacher et al.,
2005). Mechanosensory neurones do not connect directly with DMIs
in the antennal lobe (Burdohan and Comer,
1996) but branch within the deutocerebrum
(Staudacher et al., 2005),
with the DMIs passing down the VNC, ultimately activating leg motor neurones
via the TIs. Stimulation of exteroceptors at the head–scape
joint can, therefore, elicit motor output
(Burdohan and Comer, 1996;
Ritzmann and Pollack, 1994)
but preventing activation will prevent motor output.
We show that cockroaches are able to detect static electrical fields and avoid them. They do this not with a specialised detection system but by virtue of having long antennae that are easily charged and displaced by electric fields. This raises the possibility that other insects may also respond to electric fields in the same way and potentially may lead to the development of alternative measures of pest control.
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Acknowledgments |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Bell, W. J. and Adiyodi, K. G. (1981). The American Cockroach. London: Chapman & Hall.
Bindokas, V. P., Gauger, J. R. and Greenberg, B. (1988). Mechanism of biological effects observed in Honey Bees (Apis mellifera, L) hived under extra high voltage transmission lines-implications derived from bee exposure to simulated intense electric fields and shocks. Bioelectromagnetics 9, 285-301.[CrossRef][Medline]
Bullock, T. H. (1982). Electroreception. Annu. Rev. Neurosci. 5,121 -170.[CrossRef][Medline]
Burdohan, J. A. and Comer, C. M. (1996).
Cellular organization of an antennal mechanosensory pathway in the cockroach,
Periplaneta americana. J. Neurosci.
16,5830
-5843.
Camhi, J. M. and Johnson, E. N. (1999). High frequency steering manoeuvres mediated by tactile cues: antennal wall-following by the cockroach. J. Exp. Biol. 202,631 -643.[Abstract]
Chapman, C. E., Blondin, J. P., Lapierre, A. M. and Nguyen, D. H. (2005). Perception of local DC and AC electric fields in humans. Bioelectromagnetics 26,357 -366.[CrossRef][Medline]
Comer, C. M., Mara, E., Murphy, K. A. and Getman, M. (1994). Multisensory control of escape in the cockroach Periplaneta americana. 2. Patterns of touch-evoked behavior. J. Comp. Physiol. A 174,13 -26.
Comer, C. M., Parks, L., Halvorsen, M. B. and Breese-Terteling, A. (2003). The antennal system and cockroach evasive behaviour. II. Stimulus identification and localization are separable antennal functions. J. Comp. Physiol. A 189,97 -103.[Medline]
Cowan, N. J., Lee, J. and Full, R. J. (2006).
Task-level control of rapid wall following in the American cockroach.
J. Exp. Biol. 209,1617
-1629.
Durr, V., Konig, Y. and Kittmann, R. (2001). The antennal motor system of the stick insect Carausius morosus: anatomy and antennal movement pattern during walking. J. Comp. Physiol. A 187,131 -144.[CrossRef][Medline]
Edwards, D. K. (1960a). Effects of artificially produced atmospheric electrical fields upon the activity of some adult Diptera. Can. J. Zool. 38,899 -912.[Medline]
Edwards, D. K. (1960b). Effects of experimentally altered unipolar air-ion density upon the amount of activity of the blowfly, Caliphora vicina R.D. Can. J. Zool. 38,1079 -1091.[CrossRef]
Edwards, D. K. (1961). Influence of electrical field on pupation and oviposition in Nepytia phantasmaria stkr. (Lepidoptera, Geometridae). Nature 191,976 -993.[CrossRef]
Fews, A. P., Henshaw, D. L., Keitch, P. A. and Close, J. J. (1999a). Increased exposure to pollutant aerosols under high voltage power lines. Int. J. Radiat. Biol. 75,1505 -1521.[CrossRef][Medline]
Fews, A. P., Henshaw, D. L., Wilding, R. J. and Keitch, P. A. (1999b). Corona ions from power lines and increased exposure to pollutant aerosols. Int. J. Radiat. Biol. 75,1523 -1531.[CrossRef][Medline]
Gabel, C. V., Gabel, H., Pavlichin, D., Kao, A., Clark, D. A.
and Samuel, A. D. T. (2007). Neural circuits mediate
electrosensory behaviour in Caenorhabditis elegans. J.
Neurosci. 27,7586
-7596.
Gewecke, M. (1974). The antennae of insects as air current sense organs and their relationship to the control of flight. In Experimental Analysis of Insect Behaviour (ed. L. Barton Browne). Berlin: Springer.
Heiligenberg, W. and Bastian, J. (1984). The electric sense of weakly electric fish. Annu. Rev. Physiol. 46,561 -583.[CrossRef][Medline]
Hopkins, C. D. (1988). Neuroethology of electric communication. Annu. Rev. Neurosci. 11,497 -535.[CrossRef][Medline]
Hunt, E. P., Jackson, C. W. and Newland, P. L. (2005). `Electropellancy' behaviour of Periplaneta americana exposed to friction charged dielectric surfaces. J. Electrostat. 63,853 -859.[CrossRef]
Jackson, C. and McGonigle, D. (2005). Direct monitoring of the electrostatic charge of house flies (Musca domestica L.) as they walk on a dielectric surface. J. Electrostat. 63,803 -808.[CrossRef]
Kalmijn, A. J. (1971). The electric sense of
sharks and rays. J. Exp. Biol.
55,371
-383.
Kalmijn, A. J. (1982). Electric and magnetic
field detection in Elasmobranch fish. Science
218,916
-918.
Kalmijn, A. J. (1988). Detection of weak electric fields. In Sensory Biology of Aquatic Animals (ed. J. Atema, R. R. Fay, A. N. Popper and W. N. Tavolga), pp.151 -186. New York: Springer-Verlag.
Kloppenburg, P. (1995). Anatomy of the antennal motoneurons in the brain of the Honey Bee (Apis mellifera). J. Comp. Neurol. 363,333 -343.[CrossRef][Medline]
Maher, B. A. (1998). Magnetite biomineralization in termites. Proc. R. Soc. Lond., B, Biol. Sci. 265,733 -737.[CrossRef]
Maw, M. G. (1961). Behaviour of an insect on an electrically charged surface. Can. Entomol. 93,391 -393.
Maw, M. G. (1962). Behaviour of insects in electrostatic fields. Proc. Entomol. Soc. Manitoba. 18, 30-36.
Maw, M. G. (1964). An effect of static electricity on captures in insect traps. Can. Entomol. 96, 1482.
McCann, J., Dietrich, F. and Rafferty, C. (1998). The genotoxic potential of electric and magnetic fields: an update. Mutat. Res. 411, 45-86.[CrossRef][Medline]
McCann, J., Dietrich, F., Rafferty, C. and Martin, A. O. (1993). A critical review of the genotoxic potential of electric and magnetic fields. Mutat. Res. 297, 61-95.[CrossRef][Medline]
McGonigle, D. F., Jackson, C. W. and Davidson, J. L. (2002). Triboelectrification of houseflies (Musca domestica L.) walking on synthetic dielectric surfaces. J. Electrostat. 54,167 -177.[CrossRef]
Okada, J. and Toh, Y. (2000). The role of antennal hair plates in object-guided tactile orientation of the cockroach (Periplaneta americana). J. Comp. Physiol. A 186,849 -857.[CrossRef][Medline]
Okada, J. and Toh, Y. (2001). Peripheral representation of antennal orientation by the scalpal hair plate of the cockroach Periplaneta americana. J. Exp. Biol. 204,4301 -4309.[Medline]
Okada, J. and Toh, Y. (2006). Active tactile sensing for localization of objects by the cockroach antenna. J. Comp. Physiol. A 192,715 -726.[CrossRef][Medline]
Orlov, V. M. (1990). Invertebrates and high voltage power lines. J. Bioelect. 9, 121-131.
Orlov, V. M. and Babenko, A. S. (1987). Effect of the electric field of high voltage transmission lines on land invertebrates. Sov. J. Ecol. 18,267 -274.
Perumpral, J. V., Earp, U. F. and Stanley, J. M. (1978). Effects of electrostatic fields on locational preference of house flies and flight activities of cabbage loopers. Environ. Entomol. 7,482 -486.
Ritzmann, R. E. and Pollack, A. J. (1994). Responses of thoracic interneurons to tactile stimulation in the cockroach, Periplaneta americana. J. Neurobiol. 25,1113 -1128.[CrossRef][Medline]
Ritzmann, R. E. and Pollack, A. J. (1998). Characterization of tactile-sensitive interneurons in the abdominal ganglia of the cockroach, Periplaneta americana. J. Neurobiol. 34,227 -241.[CrossRef][Medline]
Ritzmann, R. E., Pollack, A. J., Hudson, S. E. and Hyvonen, A. (1991). Convergence of multimodal sensory signals at thoracic interneurons of the escape system of the cockroach, Periplaneta americana. Brain Res. 563,175 -183.[CrossRef][Medline]
Sherman, A. and Dickinson, M. H. (2004).
Summation of visual and mechanosensory feedback in Drosophila flight
control. J. Exp. Biol.
207,133
-142.
Shimizu, H. O. and Shimizu, K. (2003). Evaluation of hair displacement in ELF electric field exposure. Asia-Pacific Conf. Environ. Electromagnetics CEEM 2003,115 -117.
Shimizu, H. O. and Shimizu, K. (2004). Experimental analysis of the human perception threshold of an ELF electric field. IEEE Trans. Electron. Devices 51,833 -838.[CrossRef]
Staudacher, E. M., Gebhardt, M. and Durr, V. (2005). Antennal movements and mechanoreception: neurobiology of active tactile sensors. Adv. Insect Physiol. 32, 49-205.[CrossRef]
Watson, D. B. (1984). Effect of an electric field on insects. N. Z. J. Sci. 27,139 -140.
Watson, D. B., Sedcole, N. P., Chan, E. and Smart, K. G. (1997). The movement of insects in an electric field. 10th Int. Conf. Electromagnetic Comp.,54 -58.
Wiltschko, R. and Wiltschko, W. (2006). Magnetoreception. BioEssays 28,157 -168.[CrossRef][Medline]
Ye, S. and Comer, C. M. (1996). Correspondance
of escape-turning behaviour with activity of descending mechanosensory
interneurons in the cockroach, Periplaneta americana. J.
Neurosci. 16,5844
-5853.
Ye, S., Leung, V., Khan, A., Baba, Y. and Comer, C. M. (2003). The antennal system and cockroach evasive behaviour. I. Roles for visual and mechanosensory cues in the response. J. Comp. Physiol. A 189,89 -96.[Medline]
Yes'Kov, Y. K. and Sapozhnikov, A. M. (1976). Mechanisms and perception of electric fields by Honey Bees. Biophysics 21,1124 -1130.
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