Mechanoreceptors involved in the hindwing-evoked escape behaviour in cricket, Gryllus bimaculatus
1 Division of Biological Sciences, Graduate School of Science, Hokkaido,
University, Sapporo 060-0810, Japan
2 Kawasaki College of Allied Health Professions, Kurashiki 701-0194,
Japan
* Author for correspondence (e-mail: tetutaro{at}sci.hokudai.ac.jp)
Accepted 30 October 2002
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: cricket, Gryllus bimaculatus, mechanosensory, hindwing, escape jumping, sensilla
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
In the cricket Gryllus bimaculatus, it is well known that, as in
the cockroach Periplaneta americana
(Camhi, 1984;
Plummer and Camhi, 1981
), the
air current stimulus applied to the cerci evokes escape behaviour that
consists of running forward away from the stimulus source
(Gras and Hörner, 1992
;
Tauber and Camhi, 1995
). The
mechanosensory system that is responsible for detecting the stimulus and
transmitting the sensory information to the motor centre for escape running
has been intensively studied (Boyan et al.,
1989
; Hustert,
1978
,
1985
;
Hörner, 1992
). On the
other hand, mechanical stimulation of the hindwing elicits another type of
escape behaviour in cricket, consisting of initial jumping and subsequent
running to avoid the stimulus (Hiraguchi
and Yamaguchi, 2000
). Behavioural and electromyographic studies
have revealed that the movement pattern of legs in the initial jump is
different to that in the jump of the locust Schistocerca gregaria
(Heitler and Burrows, 1977
;
Tauber and Camhi, 1995
). Using
three types of mechanical stimuli, i.e. bending, touching with a paint brush
and pinching with fine forceps, Hiraguchi and Yamaguchi
(2000
) studied which stimulus
was most effective in eliciting the escape jumping. Although bending and
pinching were found to be equally effective in eliciting a simple response
involving kicking or running, pinching was the most effective in eliciting
escape jumping. The mechanosensory system responsible for detecting the pinch
stimulus and transmitting the information to the central nervous system,
however, remains unknown.
Many types of mechanosensory sensillae, including trichoid, campaniform and
chaetic sensillae, on the cuticular surface of the insect wing have been
reported (Elliott, 1983;
Gettrup, 1966
;
Schäffner and Koch, 1987
;
Fudalewicz-Niemczyk and Rosciszewska,
1972
). It remains to be clarified which types of mechanosensory
sensillae are present on the distal surface of hindwing.
In the present study, we investigated, by partial ablation of the vein system, which part of the hindwing was responsible for detecting the touch and pinch stimuli to elicit the escape behaviour. We used a scanning electron microscope to quantitatively examine how and what types of mechanosensory sensillae were distributed over the wing surface. By directly stimulating each of the sensillae, we studied the physiological characteristics of afferent activities. The results showed that a specific type of mechanoreceptive sensillae, having characteristic structure and responsiveness, was abundantly present on the tip region of the hindwing that was responsible for detecting the stimulus resulting in escape jumping and running.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Morphology of the hindwing
The structural characteristics of the hindwing were examined under a
dissecting microscope (SZH-131, Olympus, Tokyo, Japan). Fine details were
compared with photographs of the hindwing taken with a microscopic camera
(PM-20, Olympus). For scanning electron microscopy, the hindwing was isolated
from the rest of the body. The specimen was then fixed in 100% ethanol,
critical point freeze-dried in a vacuum evaporator, mounted on a peg and
coated with goldpalladium. A scanning electron microscope (JSM-T300,
JEOL, Tokyo, Japan) was used to compare the results of freeze-dried and
naturally dried specimens. Veins and other parts of the hindwing were named
according to Fudalewicz-Niemczyk and Rosciszewska
(1972) and Brodsky
(1994
). In this study, the
veins were numbered successively from the most anterior vein
(Fig. 1C).
|
Behavioural experiment
In order to find out which part of the hindwing was responsible for
receiving the effective stimulus for eliciting escape behaviour, selective
ablation experiments were conducted. Experimental groups included animals with
their forewings removed, those with the vannus of hindwing removed, those with
the vannus and veins (#4, #5, #6 and #9) removed, and those with the veins
(#2, #3, #7, #8 and #10) removed by cutting with scissors. The proximal half
of the hindwing was left intact. The pinching stimulus was applied to the tip
of the hindwing as described elsewhere
(Hiraguchi and Yamaguchi,
2000). Each animal was stimulated five times. The rate of
occurrence was obtained for each animal by dividing the number of responses by
the number of stimulations.
Electrophysiological recording from the wing nerve
The hindwing was isolated from the rest of the body. The cut-end was
protected against desiccation with petroleum jelly. For recording the type II
unit activity, the cuticle on the dorsal side was removed at the branching
point of veins #7 and #8 (Fig.
1C) to expose a branch of the wing nerve. A pair of hook
electrodes was placed on the branch in the vein #7 or #8 and covered with
petroleum jelly under a dissecting microscope. The electrodes were connected
to a differential amplifier (MEG-2100, Nihon-Kohden, Tokyo, Japan) whose
output was fed to an analogue oscilloscope (Tektronix 5100, Beaverton, USA)
and stored on magnetic tapes using a DAT recorder (DTR-1801, Biologic, Claix,
France; frequency range DC -20 kHz). In later analyses, the recorded signal
was replayed and fed to PowerLab/8RSP (ADInstruments, Tokyo, Japan), which was
controlled by Chart version 4.0 running on a PowerMacintosh 7300 personal
computer. For measuring the conduction velocity of sensory units, the wing
nerve between the hindwing and the metathoracic ganglion was exposed and
isolated together with the wing. Two pairs of hook electrodes were placed
along the nerve, separated from each other by approximately 2 mm. For unknown
reasons, the physiological condition of the nerve rapidly deteriorated after
exposure to saline. Thus, reliable recording was possible for less than 30
min.
In order to examine the activity of wing proprioceptors, we made a
headthorax preparation with the hindwing intact on one side
(Hiraguchi and Yamaguchi,
2000). An extracellular suction electrode was placed on the N2D2
of the metathoracic ganglion. This nerve contains only those axons from the
wing proprioceptors (Kutsch and Huber,
1989
). The pinching stimulus that was made manually with fine
forceps was monitored by measuring the electrical resistance between the
forceps and the insect body.
Mechanical stimulation
The single mechanosensory sensilla was directly stimulated with a fine
tungsten stylus (50 µm in diameter) sharpened by electrolysis. The stylus
was attached to a loud speaker (8 impedance, 0.5 W) that was driven by
the output of a hand-made amplifier with a current booster circuit. A single
cycle of sinusoidal signal was produced by a function generator (3312A,
Hewlett-Packard, Palo Alto, USA) and fed into the amplifier. The stimulus was
started at the lower reversal point of the sine wave in order to avoid sudden
movement at the onset of stimulus. The position of the stylus relative to the
sensilla was fine-tuned by DC offset of the function generator. Movement of
the stylus was monitored not by the driving signal but by a phototransistor
coupled with a light-emitting diode between which the stylus was positioned.
The stylus could follow up to 120 Hz. The stylus was placed just in contact
with the sensilla under a microscope (BX-60, Olympus) with an objective
(x20) having 7.5 mm working distance. Depending on the stylus position,
the sensilla was lifted or further lowered from its lying position during the
first half of the single sinusoidal cycle and returned to the original
position during the second half. The return of the sensilla to its original
position was due to its elasticity. The shape of the stylus was adjusted for
each hair and for stimulus direction.
In the experiment to measure the conduction velocity of sensory units associated with type I, II and campaniform sensillae, we used different types of stylus suited for stimulation of each type of sensillae and adopted pulse function with the duration of 100 ms, instead of a sinusoidal cycle, as the stimulus profile for stylus movement to activate the sensillae as securely as possible. The pulse interval was adjusted in each preparation according to the frequency of background spike discharge in order to unambiguously discriminate the elicited spikes from the spontaneous ones.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The dorsal view of the hindwing is illustrated in Fig. 1C,D. In this study, the veins were numbered successively from the most anterior vein (Fig. 1C). Six of the veins (#1, #2, #3, #7, #8 and #10) were thick, having a rather massive, brownish cuticular layer. The thin cuticular membrane between veins was partitioned into several cells by cross veins (Fig. 1D). Between veins #7 and #8, the membrane was made of thick cuticle. The cells were numbered successively from the most distal cell. The tip of the forewing that overlapped with the hindwing was located at the level of the 17th or 18th cell (17.7±0.2; mean ± S.E.M., N=5). Proximal cells were entirely covered by the forewing. The costa, i.e. vein #1, was isolated from the rest of the hindwing veins at its basal part, being shorter than the other veins. Veins #2-#9 branched out from a few veins at the basal part of the hindwing and extended to the distal part of the hindwing. Vein #10 emerged from another vein at the basal part. They were placed next to each other when the hindwing was folded. In the middle part of the folded hindwing, six veins (#2, #3, #4, #7, #8 and #10) were placed on the most dorsal side, and only two of them (#7 and #8) were on the most dorsal side in the distal part of the folded hindwing. Veins #7 and #8, together with the membrane between them, were directly exposed to the external world.
Role of proprioceptors in evoking escape behaviour
It has been reported that many kinds of proprioceptors are located at the
base of the hindwing and in the thorax
(Altman and Tyrer, 1974;
Gettrup, 1966
) to detect the
position and movement of the hindwing. In order to test the possibility that
they trigger the escape behaviour in response to mechanical stimulation of the
hindwing, we immobilized the proximal part of the hindwing (approximately
two-thirds of the whole wing) by fixing it to the abdominal tergum with a
piece of cover glass using wax. The glass was used to prevent, by its own
weight, transmission of the wing movement caused by pinching stimulation to
thoracic proprioceptors. The distal half of the forewing was removed. Each of
10 experimental animals was stimulated five times, with an interval between
stimulations of at least 3 min, by single pinching applied manually to the
hindwing tip. The rate of response was obtained for each animal by dividing
the number of responses by the number of stimulations. The rate of occurrence
of escape behaviour in response to pinching stimulus in the experimental
animals (82.0±6.5%) was not statistically different
(P>0.05; Student's two-sided unpaired t-test;
Fig. 2A) from that in intact
animals (90.0±3.3%). The result indicated that the sense organs
responsible for detecting the mechanical stimulus applied to the hindwing to
elicit escape behaviour were present not at the base but on the surface of the
hindwing. We also confirmed physiologically that pinching stimuli evoked no
significant response of the proprioceptors in either the intact or fixed
condition (Fig. 2B,C; N=6).
|
The branching pattern of veins in the hindwing is illustrated in
Fig. 2D. Six thick veins were
located in the remigium region. Of these, veins #7 and #8 were the longest. In
animals with their forewings ablated, removing a specific region of the
hindwing significantly affected the occurrence of escape behaviour elicited by
the pinching stimuli applied to the tip of the hindwing
(Fig. 2E). When the vannus of
hindwing was totally removed (group `a' in
Fig. 2E), the rate of
occurrence was 94.0±4.2% (N=10 animals). When the vannus and
veins #4, #5, #6 and #9 were removed (group `b'), the occurrence rate was
96.0±2.6% (N=10 animals). When veins #2, #3, #7, #8 and #10
were removed (group `c'), however, the average rate of occurrence was
8.0±5.3% (N=10 animals). The difference in the rate of
occurrence among the three groups was statistically significant
(P<0.001; single classification ANOVA). Planned comparisons among
pairs of means (Sokal and Rohlf,
1995) revealed that the occurrence rate for group `c' was
significantly lower than the rate for groups `a' and `b' (P<0.001
for both). These results suggested that the mechanosensory organs for
detecting the stimuli to elicit escape behaviour were located on veins #2, #3,
#7, #8 and #10.
Sensillae on the hindwing surface
Scanning electron microscopy has revealed that there are several types of
hair-like structure on the cuticular surface of the hindwing. In the remigium
region of the hindwing, we identified three types of sensory hair structure
that existed on some of the veins and cross veins and on the specific part of
membranous cells surrounded by them. The observation that these hairs rested
on a socket-like structure suggested that they were all mechanosensory
sensillae. In this study, those hairs with a smooth and thread-like shaft were
classified as type I sensillae. They were all longer than 100 µm (mean
± S.E.M., 264.0±11.0 µm, N=50 from six wings;
Fig. 3A,B) and their morphology
resembled that of sensillae on the cerci of the cricket and locust
(Boyan et al., 1989;
Gnatzy and Hustert, 1989
;
Murphey, 1985
) as well as on
the body and appendage surface of other arthropods
(Gronenberg and Tautz, 1994
).
Those hairs with a stout and bristle-like shaft were designated as type III
sensillae (Fig. 3C,D). Being
short in length (45.5±1.0 µm, N=50 from five wings), they
appeared to correspond to the bristle sensillae reported in the cricket
(Boyan et al., 1989
;
Hamon and Guillet, 1996
;
Murphey, 1985
), The
length-distribution histogram (Fig.
3E) showed that type I sensillae were discontinuously longer than
other sensillae, including type III sensillae.
|
In the present study, for the first time, we found hairs with a shaft that
was characteristically twisted and typically resting in a deflected position,
paralleling or making contact with the cuticular surface
(Fig. 4). They were relatively
small at low magnification (Fig.
4A), but observation under higher magnification revealed their
twisted structure (Fig. 4B).
Statistical association between the twisted structure and the hair length was
demonstrated to be significant using a 2 test
(P<0.001), indicating that the two populations of hairs, either
having or lacking the twisted structure, were different in their hair length.
Although the hair shown in Fig.
4B looks like it is standing straight up from the cuticular
surface, it was in reality deflected towards the surface, as shown in
Fig. 4C. No sensory hair
structures so far reported in other mechanosensory systems appear to
correspond to the type II sensillae. They were significantly shorter
(10.4±0.2 µm, N=50 from five wings) than both type I and
type III sensillae (P<0.01 for both; Student's two-sided unpaired
t-test). As campaniform sensillae are well known for reception of
cuticular distortion (Schäffner and
Koch, 1987
), which is likely to be caused by pinch stimulation, we
looked for this type of sensilla carefully in this study. However, no evidence
was found that they were present on the hindwing tip.
|
We have counted under a microscope the number of mechanosensory hairs on the cell surface between, and including, veins #7 and #8 using five wings from five animals. It was found that type II sensillae were most abundant on the surface of the middle to distal region, i.e. the sixth and seventh cells from the most distal cell, decreasing in number both in the proximal and distal directions: there were approximately 22 type II sensillae on the seventh cell compared with two sensillae on the most distal cell and on a proximal (i.e. 20th) cell (Fig. 5A). They were mostly confined to the distal part of each cell on its dorsal side (Fig. 8). No other veins apart from #7 and #8 were found to carry type II sensillae. These sensillae were also distributed on the surface of veins #7 and #8 uniformly over their length on the hindwing (Fig. 5B). By contrast, type I sensillae were found to exist only on the proximal region. Type III sensillae were only scarcely present on the surface of all cells, with a mean number of 1.9±0.2 sensillae on each cell (Fig. 5C).
|
|
Conduction velocity
In order to measure the conduction velocity of sensory nerves associated
with the type II sensillae, we stimulated the sensillae and made extracellular
recordings from the nerve axon using two pairs of hook electrodes. For
comparison, we also measured the conduction velocity of nerves associated with
type I and campaniform sensillae. In the experiments illustrated in
Fig. 6A-C, each type of
sensillae was selectively stimulated and their nerve activity was recorded at
two different sites along the wing nerve
(Fig. 6D) using two pairs of
hook electrodes separated from each other by approximately 2 mm. As the
campaniform sensillae were not found on the hindwing tip region, we stimulated
those found on the proximal part of the hindwing. The location of stimulated
sensillae is shown schematically in Fig.
6D. For recording type I unit activity, the wing nerve was severed
distally to the site of stimulation in order to make the unit activity
discernible from reduced spontaneous spike discharges
(Fig. 6A). In other recordings,
the whole hindwing nerves remained intact: the type II and campaniform unit
activities were observed among many spontaneous spikes but were unambiguously
discernible as they were locked to the stimulus onset
(Fig. 6B) or onset and offset
(Fig. 6C). Since we
simultaneously stimulated several sensillae of the same type for reliable
recording of the unit activity, several units were observed to be activated in
a single stimulation (Fig.
6A-C). We selected one or two discernible units and measured their
conduction velocity by dividing the distance between electrodes by the delay
time.
|
The conduction velocity of type I, type II and campaniform units is summarised in Fig. 6E. The conduction velocity of the type I unit (2.4±0.5 m s-1; N=10 units from eight animals) was found to be as fast as that of the campaniform unit (2.3±0.1 m s-1; N=5 units from three animals; P>0.05, Student's two-sided t-test), whereas the conduction velocity of the type II unit (1.4±0.1 m s-1; N=6 units from six animals) was significantly slower than those of the other types of units (P<0.05). In accordance with its high conduction velocity, the type I unit showed significantly large spike amplitude (465.1±20.0 µV; P<0.05) compared with that of the type II unit (177.6±7.9 µV). The spike amplitude of the campaniform unit (334.9±8.4 µV) was not statistically different from that of the type I unit (P>0.05). The difference between the spike amplitudes of the type II and campaniform sensillae was statistically significant (P<0.05).
Afferent responses to stimulation of a single type II sensilla
For studying the response characteristics of type II sensillae, we adopted
sinusoidal stimulation, instead of the rectangular stimulation adopted in the
preceding experiment (Fig. 6).
A single type II sensilla was deflected sinusoidally, using one cycle starting
from the minimum point at varying frequency (0.1-120 Hz). Each stimulation was
separated by an interval of 60 s. When the sensilla was lifted from and
returned to its initial lying position
(Fig. 7A), almost no spike
discharge was observed at low frequencies (<1 Hz). At higher frequencies,
the sensory nerve connected with the sensilla usually responded with a single
or a few spikes. The spike response was always phasic: sustained spike
discharge was never observed in this study, although the sensilla remained
deflected for a while during stimulation. When the cuticular surface in the
vicinity of the sensilla was directly stimulated, no response was recorded
(Fig. 7A). Since the recording
electrode was placed several mm away from the sensilla, the relative timing of
spike discharge to the stimulus monitor varied depending on the stimulus
frequency. Even with the same stimulus frequency, the timing of spike
discharge showed fluctuation, as exemplified in the responses to 10 Hz
stimulation in Fig. 7A. The
fluctuation was also observed when the sensilla was lifted from and returned
to the original position (Fig.
7B). The timing of spike discharge fluctuated over a range of >
10 ms in 10 Hz stimulation. These observations suggested that activation of
the sensory unit associated with the type II hair would not be strictly
related to its deflection angle or direction. It thus appeared that a single
type II sensilla would not encode detailed information on the stimulus;
instead, it would carry general information on whether the stimulus to the
hindwing tip is present or not when the stimulus is fast enough (> 1
Hz).
|
It was also noted that the response of a single type II unit to repeated stimulation was of probabilistic nature (Fig. 7C). When the stimulus of the same frequency and amplitude was repeated 10 times, the probability of spike discharge increased with the stimulus frequency up to about 0.7±0.1 at 10 Hz (N=100 in 10 animals). At frequencies higher than 10 Hz, the probability remained unchanged except at 50 Hz. The finding that the maximal probability of spike discharge in response to stimulation was approximately 0.7 indicated that a single type II sensilla by itself would not be able to detect the stimulus with adequate precision for eliciting escape jumping. This disadvantage appears to be compensated for by high-density distribution of type II sensillae on the hindwing tip region (see Discussion).
We also examined the response characteristics of 12 type II sensillae in the same preparation (Fig. 8). Most of them (11/12) responded to more than three out of five stimulation trials with a single or a few spikes. None of the examined units in this experiment responded with spike discharge to every trial of stimulation. One hair, shown in the top-left corner in Fig. 8, never caused spike discharge upon stimulation. This failure appeared to be due to inadvertent damage to the nerve or to unfavourable axon location within the nerve for the recording electrode. The latent period from the stimulus onset to the first spike discharge in Fig. 8 ranged from 26.4 ms to 28.9 ms (mean ± S.E.M., 27.8±0.2 ms). This variability was partly due to unintentional differences in the positioning of the stylus for each hair but also appeared to reflect the unstable timing of spike discharge in response to deflection of the same hair (Fig. 7). Although a single type II unit was not reliably responsive to hair deflection even within the preferred frequency range, we concluded that the animal would be able to respond with escape jumping to the stimulus applied to the hindwing tip by monitoring the spike activity of a population of type II sensillae that are present almost exclusively and close together on the exposed surface of the hindwing.
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Hindwing as the sensory organ
There are many studies to date about the insect wing as the flight organ
(Ellington, 1991;
Brodsky, 1994
). Studies on the
sensory function of the wing have been mostly focused on mechanoreceptors
related to flight control. Many types of receptors have been reported on or in
the wings: filiform and campaniform sensillae on the basal part of the
forewing (Fundalewicz-Niemczyk and Rosciszewska, 1972;
Elliott et al., 1982
) and
stretch receptors attached to the forewing hinge (Schäffner and Koch,
1986; Gettrup, 1966
). In
flying insects, those sensory organs detecting the distortion of the wing in
the proximal part of hindwings during flight have been studied in detail
regarding their morphology and physiology
(Yack and Fullard, 1993
).
Although Matheson (1997
,
1998
) reported that
stimulation of hindwing tactile receptors elicited scratching movements of a
hind leg in locusts, the sensory function of hindwings largely remains to be
thoroughly examined.
The field cricket Gryllus bimaculatus has a relatively longer pair
of hindwings than forewings (Fig.
1A,C), with a vein diversion pattern as simple as that of
primitive species (Brodsky,
1994). It has many long and straight veins, and a lot of short,
straight cross veins. Almost an entire portion of the hindwing is covered by
the forewing, only the distal part being exposed to the external environment
in Gryllus. In the present study, we found that a new sensory system
resided on this part of the hindwing. The results suggested that the hindwing
would play an important and unique role in controlling behaviour, acting
together with antennae and cerci.
Reception site of mechanical stimulation
We demonstrated by immobilization experiments
(Fig. 2) that the
mechanosensory stimulus applied to the hindwing tip to elicit escape jumping
was received by exteroceptors on the hindwing rather than proprioceptors at
its base or in the thorax. By immobilizing the hindwing and ablating the whole
forewing, we found that the distal part of the hindwing would play an
important role in detecting the mechanical stimuli. Partial ablation of the
hindwing vein system further showed that the mechanosensory receptors
responsible for receiving the escape-eliciting stimuli were mostly distributed
on veins #7 and #8 (Fig. 2B).
Examination of the cuticular surface of the hindwing using a scanning electron
microscope revealed three morphological types of sensory hairs. Type I and
type III hairs (Figs 3,
4) appeared to be the same as
filiform (Gnatzy and Hustert,
1989; Murphey,
1985
) and bristle sensillae
(Boyan et al., 1989
;
Hamon and Guillet, 1996
),
respectively. Type II hairs, in contrast, appeared to be a novel type, as no
known sensillae in insect correspond to these hairs
(Mclver, 1985
;
Schwartzkopff, 1964
). It
should be noted here that, although we did not encounter other types of
sensillae in the present study, this does not entirely exclude the possibility
that, for example, campaniform sensillae or internal multipolar receptors
might also be present. Further study is needed to test this possibility.
Quantitative observation has revealed that the type II sensillae were more abundant than the other two types of sensillae on the membranous cells between veins #7 and #8 in the distal to middle regions. Type I sensillae were found only in the proximal region of the hindwing on the veins #1-#9. Type III sensillae were very sparse throughout the membrane between veins #7 and #8 (Fig. 5). These findings suggest that type II sensillae are responsible for detecting the mechanosensory stimuli and transmitting the sensory information to the central nervous system.
Morphological characteristics of type II sensillae
Compared with the filiform sensillae on cerci, which have been reported to
be involved in detection of wind stimuli in crickets, the type II sensillae on
the hindwing are significantly shorter (10.4±0.2 µm; filiform
sensillae, 158.0±6.8 µm). Characteristic to the type II sensillae
was the twisted shaft (Fig. 4).
Grooves on the shaft surface running in the axial direction clearly indicate
the twisted structure. The whole shaft was most typically deflected at rest,
paralleling or making contact with the cuticular surface. We think that these
structural characteristics of type II sensillae are not artifacts but reflect
their original morphology, as filiform sensillae, termed type I in this study,
generally stood up vertically on the cuticle with straight external appearance
in the same preparation. The type II sensillae (10.4±0.2 µm in shaft
length) were found to be significantly shorter (P<0.01) than type
I (264.0±11.0 µm) and type III (45.5±1.0 µm)
sensillae.
Filiform sensillae on the cerci of Gryllus bimaculatus have been
reported to range from approximately 30µm to 1500 µm in length, thus
having compatible length with type I sensillae on the hindwing tip
(Fig. 3A-C). The cercal
sensillae are receptive for air current stimuli
(Dumpert and Gnatzy, 1977;
Boyan et al., 1989
): depending
on the hair length, filiform hairs are thought to be specialised in detecting
wind velocity or acceleration (Kanou and
Shimozawa, 1984
; Shimozawa and
Kanou, 1984b
). Having a short and crooked shaft, rather than the
long and straight shaft of wind-sensitive filiform hairs, the type II
sensillae (Fig. 4) are unlikely
to be receptive for air current stimuli. The fact that in some cases the type
II hair shaft was in contact with the cuticular surface further supported this
possibility. In the course of this study, we actually observed that wind
stimulation applied to the hindwing tip elicited no reliable response (data
not shown). The morphology of type II sensillae also suggested that the
adequate stimulus for them would be touching or direct bending by an external
object. Such mechanoreceptive sensillae that are activated by direct bending
are also well known in insects (Brown and
Anderson, 1998
; Gaffal and
Theiß, 1978
; Gnatzy and
Hustert, 1989
; Klein,
1981
; Murphey,
1985
).
Physiological characteristics of type II sensillae
Characteristic to the physiology of type II sensillae was that the sensory
units associated with the sensilla did not respond reliably to mechanical
stimulation: in the experiment shown in
Fig. 7C, the maximal
probability of response was approximately 0.7, indicating that the unit would
fail to respond to the stimulus three times in every 10 cases. This
unreliability might have been caused by inadequate stimulation in the present
study: the twisted and bent structure of the type II sensilla
(Fig. 4) made sure stimulation
relatively difficult. The unreliability observed in the type II unit response
might therefore reflect that of stimulation. The situation that the type II
sensillae have a shape that is not suited for receiving point stimuli,
however, holds true in the natural environment as well as in the laboratory.
Thus, a sharp and pointed object in the natural surroundings of the cricket
would not be able to effectively stimulate any single type II sensilla on the
hindwing. Furthermore, also characteristic of the physiology of type II
sensillae was that the timing of spike discharge in relation to sinusoidal
stimulation of the sensilla was not precisely locked to the stimulus but
considerably variable (Figs 7,
8). This variability might also
be due to the difficulty in stimulation described above. But the difficulty
would also be encountered by natural stimulation. The type II sensillae system
would thus be unable to detect the precise direction of natural stimuli
applied to the hindwing. These physiological characteristics of a single type
II sensilla, not favourable for accurate detection of external stimuli,
appeared to be compensated for by localized distribution of the sensillae on
the hindwing tip. Even if several sensillae fail to respond, others could
detect the presence of a specific object as far as it is not pointed but has
some effective area for contact stimulation.
Although the response characteristics of the type II sensillae remain
unknown at frequencies higher than 120 Hz
(Fig. 7C), the present study
suggests that the sensillae would not respond to slow or sustained stimuli
(<1 Hz). Type II sensillae would thus operate as a low-cut filter but,
apart from this function, they do not appear to be tuned for detection of any
specific aspect of mechanosensory stimuli. The result that type II sensillae
are generalists for detection of local mechanosensory stimuli rather than
specialists for any particular stimulus parameters seems to be consistent with
the result of behavioural analyses
(Hiraguchi and Yamaguchi,
2000) that no specific stimulus profile was noticed in
experimental elicitation of the hindwing-evoked escape jumping.
The finding that the type II unit showed a relatively slow conduction
velocity (Fig. 6) appears to be
inconsistent with the hypothesis that it is involved in escape jumping, which,
in general, should be carried out as quickly as possible. It should be noted
here, however, that the type II sensillae are activated by contact stimuli,
i.e. pinching and touching (Hiraguchi and
Yamaguchi, 2000). This is in contrast to the cercal sensillae,
which are activated by distant stimuli, i.e. air current, to evoke escape
running from the predator (Murphey,
1985
). Hence, one possibility would be that the response time is
not critical for escape jumping: it may be elicited in natural conditions by
nonlethal stimuli such as biting by nearby conspecifics or hitting by soil
lumps. The deflected shaft of type II sensillae
(Fig. 4) would be advantageous
to protect themselves from snapping against such mechanical stimulation.
Further study is needed to test this possibility by careful observation of
cricket behaviour in their natural habitat.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Altman, J. S. and Tyrer, N. M. (1974). Insect flight as a system for the study of the development of neuronal connections. In Experimental Analysis of Insect Behavior (ed. L. Barton Browne), pp. 159-179. Heidelberg: Springer.
Boyan, G. S., Williams, J. L. D. and Ball, E. E. (1989). The wind-sensitive cercal receptor/giant interneuron system of the locust, Locusta migratoria. J. Comp. Physiol. A 165,495 -510.
Brodsky, A. K. (1994). The Evolution of Insect Flight. Oxford: Oxford University Press.
Brown, P. E. and Anderson, M. (1998). Morphology and ultrastructure of sense organs on the ovipositor of Trybliographa rapae, a parasitoid of the cabbage root fly. J. Insect Physiol. 44,1017 -1025.[CrossRef][Medline]
Camhi, J. M. (1984). A case study in neuroethology: the escape system of the cockroach. In Neuroethology: Nerve Cells and the Natural Behaviour of Animals, pp. 79-105. Sunderland, MA: Sinauer Associates.
Camhi, J. M. and Tom, W. (1978). The escape behavior of the cockroach Periplaneta americana. I. Turning response to wind puffs. J. Comp. Physiol. 128,193 -201.
Dumpert, K. and Gnatzy, W. (1977). Cricket combined mechanoreceptors and kicking response. J. Comp. Physiol. 122,9 -25.
Elliott, C. (1983). Wing hair plates in crickets: physiological characteristics and connections with stridulatory motor neurones. J. Exp. Biol. 107, 21-47.
Elliott, C., Koch, U., Schäffner, K. H. and Huber, F. (1982). Wing movements during cricket stridulation are affected by mechanosensory input from wing hair plates. Naturwissenschaften 69,288 -289.
Ellington, C. P. (1991). Aerodynamics and the origin of insect flight. Adv. Insect Physiol. 23,171 -210.
Fudalewicz-Niemczyk, W. and Rosciszewska, M. (1972). The innervation and sense organs of the wings of Gryllus domesticus L. (Orthoptera). Acta Biol. Cracov Ser. Zool. 16,35 -51.
Gaffal, K. P. and Theiß, J. (1978). The tibial thread-hairs of Acheta domesticus L. (Saltatoria, Gryllidae). The dependence of stimulus transmission and mechanical properties on the anatomical characteristics of the socket apparatus. Zoomorphologie 90,41 -51.
Gettrup, E. (1966). Sensory regulation of wing twisting in locust. J. Exp. Biol. 44, 1-16.[Medline]
Gras, H. and Hörner, M. (1992). Wind-evoked escape running of the cricket Gryllus bimaculatus. I. Behavioural analysis. J. Exp. Biol. 171,189 -214.
Gnatzy, W. and Hustert, R. (1989). Mechanoreceptors in behavior. In Cricket Behavior and Neurobiology (ed. F. Huber, W. Loher and T. E. Moore), pp.198 -226. Ithaca: Cornell University Press.
Gronenberg, W. and Tautz, J. (1994). The sensory basis for the trap-jaw mechanism in the ant Odontomachus bauri.J. Comp. Physiol. A 174,49 -60.
Hamon, A. and Guillet, J. C. (1996). Location and dynamic properties of the spike generator in an insect mechanosensory neuron. J. Comp. Physiol. A 179,235 -243.
Heitler, W. J. and Burrows, M. (1977). The locust jump. I. The motor programme. J. Exp. Biol. 66,203 -219.[Abstract]
Hiraguchi, T. and Yamaguchi, T. (2000). Escape behavior in response to mechanical stimulation of hindwing in cricket, Gryllus bimaculatus. J. Insect Physiol. 46,1331 -1340.[CrossRef][Medline]
Hörner, M. (1992). Wind-evoked escape running of the cricket Gryllus bimaculatus. II. Neurophysiological analysis. J. Exp. Biol. 171,215 -245.
Hustert, R. (1978). Segmental and interganglionic projections from primary fibers of insect mechanoreceptors. Cell Tissue Res. 194,337 -351.[Medline]
Hustert, R. (1985). Multisegmental integration and divergence of afferent information from single tactile hairs in a cricket. J. Exp. Biol. 118,209 -227.
Kanou, M., Osawa, T. and Shimozawa, T. (1988). Ecdysial growth of the filiform hairs and sensitivity of the cercal sensory system of the cricket, Gryllus bimaculatus. J. Comp. Physiol. A 162,573 -579.
Kanou, M. and Shimozawa, T. (1984). A threshold analysis of cricket cercal interneurons by an alternating air-current stimulus. J. Comp. Physiol. A 154,357 -364.
Klein, U. (1981). Sensilla of the cricket palp. Fine structure and spatial organization. Cell Tissue Res. 219,229 -252.[Medline]
Krasne, F. B. and Wine, J. J. (1987). Evasion responses of the crayfish. In Aims and Methods in Neurobiology (ed. D. M. Guthrie), pp.10 -45. Manchester: University of Manchester Press.
Kutsch, W. and Huber, F. (1989). Neural basis of song production. In Cricket Behaviour and Neurobiology (ed. F. Huber, W. Loher and T. E. Moore), pp.262 -309. Ithaca: Cornell University Press.
Matheson, T. (1997). Hindleg targeting during
scratching in the locust. J. Exp. Biol.
200,93
-100.
Matheson, T. (1998). Contralateral coordination and retargeting of limb movements during scratching in the locust. J. Exp. Biol. 201,2012 -2032.
Mclver, S. B. (1985). Mechanoreception. In Comprehensive Insect Physiology, Biochemistry and Pharmacology. vol. 6 Nervous System: Sensory (ed. G. A. Kerkut and L. I. Gilbert), pp.71 -132. New York: Pergamon.
Murphey, R. K. (1985). A second cricket cercal sensory system: bristle hairs and the interneurons they activate. J. Comp. Physiol. A 156,357 -367.
Plummer, M. R. and Camhi, J. M. (1981). Discrimination of sensory signals from noise in the escape system of the cockroach: the role of wind acceleration. J. Comp. Physiol. A 142,347 -357.
Schäffner, K. H. and Koch, U. T. (1987). A new field of wing campaniform sensilla essential for production of the attractive calling song in cricket. J. Exp. Biol. 129, 1-23.
Schwartzkopff, J. (1964). Mechanoreception. In The Physiology of Insecta I (ed. M. Rockstein), pp.509 -561. New York, London: Academic Press.
Shimozawa, T. and Kanou, M. (1984a). The aerodynamics and sensory physiology of range fractionation in the cercal filiform sensilla of the cricket Gryllus bimaculatus. J. Comp. Physiol. A 155,495 -505.
Shimozawa, T. and Kanou, M. (1984b). Varieties of filiform hairs: range fractionation by sensory afferents and cercal interneurons of a cricket. J. Comp. Physiol. A 155,485 -493.
Sokal, R. R. and Rohlf, F. J. (1995). Biometry. Third edition. New York: W. H. Freeman & Co.
Stumpner, A. and von Helversen, D. (2001). Evolution and function of auditory systems in insects. Naturwissenschaften 88,159 -170.[CrossRef][Medline]
Tauber, E. and Camhi, J. M. (1995). The
wind-evoked escape behaviour of the cricket Gryllus bimaculatus:
integration of behavioural elements. J. Exp. Biol.
198,1895
-1907.
Wine, J. J. (1984). The structural basis of an innate behavioural pattern. J. Exp. Biol. 112,283 -319.
Yack, J. E. and Fullard, J. H. (1993). Proprioceptive activity of the winghinge stretch receptor in Manduca sexta and other atympanate moths: a study of the noctuoid moth ear B cell homologue. J. Comp. Physiol. A 173,301 -307.
Related articles in JEB: