Wing hair sensilla underlying aimed hindleg scratching of the locust
Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK
* Author for correspondence (e-mail: kp231{at}cam.ac.uk)
Accepted 17 May 2004
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Summary |
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The different hair types are defined by their morphology and innervation. The shortest hairs (1446 µm) are basiconic receptors containing both chemosensory and mechanosensory afferents. They are distributed widely across the dorsal surfaces of the forewings; some are located on the ventral surfaces of the hindwings, but none are found on the ventral surfaces of the forewings or the dorsal surfaces of the hindwings. Medium length hairs (73159 µm) are found on all wing surfaces, but are restricted to the veins, principally the subcosta on the dorsal surface of the forewings. The longest hairs (316511 µm) are found only on the postcubitus vein on the dorsal surfaces of the forewings, so that they form a pair of dorsal rows when the wings are folded at rest.
Touching the dorsal surface of a forewing can elicit aimed scratching movements of a hindleg, and we show that the probability of eliciting a scratch differs for different stimulus sites and for different start positions of the hind leg. The effectiveness of different stimulus sites can be correlated with the distribution of tactile hairs on the dorsal forewing surface. Touching the long hairs provides the strongest drive to elicit a scratch, and ablating them reduces the probability to almost zero. We conclude that input from forewing tactile hairs plays an important role in eliciting hindleg scratching and encodes the spatial location required for targeting.
Key words: Schistocerca gregaria, wing, tactile hair, basiconic sensillum, scratching
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Introduction |
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In contrast to our detailed knowledge about the anatomy, physiology and
behavioural roles of trichoid hairs on the body and legs (e.g.
Burrows, 1996), surprisingly
little is known about the hairs on the wings. Each locust hindwing possesses
12 400 hairs and bristles scattered across its veins and membrane
(Altman et al., 1978
). Only
some 800 of these are innervated, and their sensory neurones project as small
diameter axons in nerve 1A into the metathoracic ganglion
(Altman et al., 1978
). The
forewings are smaller than the hindwings and have a thickened cuticle. At rest
they protect the delicate hindwings that lie folded beneath them
(Wootton et al., 2000
). The
distribution and innervation of trichoid hairs on the forewings of locusts has
not been described satisfactorily.
The single study of the forewing hairs of a locust (Locusta
migratoria), described only one type of small trichoid hair, up to 40
µm long, which were restricted to the principal veins
(Knyazeva, 1970). Hairs of
over 100 µm length were recorded on the tegulae and articular sclerites,
whereas hairs of over 300 µm were only present on the cuticle of the
pterothorax (Knyazeva, 1970
).
In contrast, our observations of ten specimens of Locusta migratoria
provided by a commercial supplier (Blades Biological, Edenbridge, UK) revealed
hairs of up to 215±37.6 µm on veins near the leading edge of the
forewing (K.P., personal observations). The trichoid hairs on the forewing
surface were assumed by Knyazeva
(1970
) to "have some
significant role for flight and [to] perceive the pressure of the air stream
on the moving wing", although this was not tested. Since the
numbers of strain-sensitive campaniform sensilla on the wings and tegula, and
tegula hairs, are generally higher in good fliers than in species with poor
flying ability, the presence of these wing receptors has been linked to the
control of flight behaviour (Knyazeva,
1986a
,b
).
This assumed role in flight is repeated in studies of the wing hairs of the
cricket Gryllus domesticus
(Fudalewicz-Niemczyk and Rosciszewska,
1972
), the grasshopper Melanoplus sanguinipes (Albert,
1976), and in a series of studies by Knyazeva on grasshopper Stauoderus
biguttulus (Za
wilichowski,
1934b
); stonefly Isopteryx tripunctata
(Za
wilichowski, 1936
),
and cockroaches Phyllodromia germanica
(Za
wilichowski, 1934a
)
and Periplaneta americana (Knyazeva, 1976a). In the nocturnal
cockroach Phyllodromia germanica the many wing hairs were suggested
to have chemosensory and mechanosensory roles (Knyazeva, 1934), but in
Periplaneta americana, since both the hairs and the campaniform
sensilla are restricted to the wing veins, which are axes of mechanical
strength, Knyazeva (1976a,b) speculated that these wing hairs might have a
role in flight.
The small axon diameters and low conduction velocities of the sensory
neurones that innervate hairs on the hindwing, and presumably also those on
the forewing, make it unlikely that these receptors are involved in rapid
reflex control or tuning the flight motor pattern on a single wing-beat time
scale (Gettrup, 1965;
Burrows, 1996
). Little is known
of the activity of forewing hair afferents during flight
(Wilson, 1961
;
Gettrup, 1965
). The synaptic
connections made by trichoid hair afferents from the locust forewing have not
been described, so it is unclear whether their signals are primarily used by
leg motor networks, flight control networks or both. Some exteroceptive
sensory inputs from the forewings, however, have been shown to converge along
with proprioceptive inputs from the ipsilateral hindleg onto spiking local
interneurones from a population that is involved in generating leg reflexes
(Matheson, 2002
).
Touching a forewing or a hindwing of a locust can elicit an aimed grooming
behaviour in which one or both hindlegs move towards the point of stimulation,
often in a cyclical trajectory (Meyer,
1993; Berkowitz and Laurent,
1996a
; Matheson,
1997
,
1998
, 2003). This scratching
behaviour might help to keep the wing surface clean or it might enable a
locust to fend off a predator or conspecific. The wing receptors underlying
aimed scratching have not been demonstrated, but the most likely candidates
are the trichoid hairs, since no other receptors are distributed across the
surface in a way that could easily signal the location of a touch. In
crickets, touching the surface of a hindwing can elicit an escape response,
which is mediated by one class of twisted trichoid hairs (Hiraguchi and
Yamaguchi, 2003).
In this paper we describe the distribution of three classes of trichoid hairs on the wings of the locust Schistocerca gregaria. We show that, of these, a row of the longest tactile hairs on the forewings was particularly effective in eliciting hindleg scratching. Stimulation of the other tactile hairs can also elicit scratching, but stimulation of the chemoreceptive afferents in basiconic receptors was relatively ineffective.
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Materials and methods |
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The forewings of females are longer than those of males, so hair counts were expressed as hairs per cm. Basiconic sensilla are not restricted to longitudinal veins, so their counts were expressed as hairs per cm2. Photographs were taken using a Nikon E995 (Kingston, UK) Coolpix digital camera attached to a dissection microscope.
Structure of exteroceptors
Individual forewings were removed from another five female locusts, rinsed
in distilled water in a sonicator to remove dust and debris, and then dried at
room temperature. Small (5 mm square) portions were then dry-mounted on
aluminium stubs, sputter-coated with gold, and examined using a Philips
(Croydon, UK) scanning electron microscope (SEM). Forty-six hairs on the
dorsal surface were photographed and their lengths measured. Care was taken to
adjust the angle of view so that it was orthogonal to the axis of each hair
measured. The distribution of hair lengths formed the basis for the three
length categories used in this paper.
Physiological recordings
Isolated fore- and hindwings were secured in modelling clay. Hair afferents
were stimulated and recorded using a modification of the `tip recording'
technique (Hodgson, 1955). A reference electrode was placed into the main wing
vein at the cut base of the wing, and a broken glass microelectrode, filled
with locust saline (or saline with additional sodium chloride to 100 mmol
l1, and sucrose to 250 mmol l1) was placed
over the intact hair tip. Signals were recorded using standard amplifiers and
captured to computer using a CED1401 interface and Spike2 software (Cambridge
Electronic Design, Cambridge, UK). Basiconic receptors were easily identified
by their multiple innervation, reflected in multiple spike amplitudes in
recordings from intact receptors. If no response was detected from an intact
hair, then it was classed as being not basiconic and its tip was cut off
before another recording was attempted. Mechanosensory hairs were recognised
by spikes of a single amplitude in response to movements of the recording
electrode. If cutting the hair shaft failed to reveal spiking activity then
the hair was cut closer to the cuticle and recording attempted again. In the
absence of activity the hair was classed as non-innervated. Over 50 recordings
were made from short hairs, severed medium length hairs, severed long hairs
and non-innervated hairs across both surfaces of fore- and hindwings of 8
animals.
Probability of eliciting a scratch
Five male and five female locusts were tethered using a wire noose around
the pronotum, and each given a polystyrene ball of 5 cm diameter, on which
they could walk freely (Matheson,
1997). The eyes and ocelli were blacked out using water-based
black acrylic paint (Daler-Rowney, Acryla; Bracknell, UK). The ten animals
were set up together and allowed to rest for 30 min before the experiment
began. A 3 mm diameter start pole provided a footrest on which the right-hand
hindleg tarsus stood at the beginning of each stimulus. This start pole was
positioned at 2/5 (anterior position) or 4/5 (posterior position) of the
distance between the metathoracic coxal joint and the distal tip of the wing,
ventral to the abdomen (Dürr and
Matheson, 2003
). The wing area was subdivided notionally along the
proximaldistal axis (which lies anteriorposteriorly when the
wings are folded at rest) into five bins of equal length, the four most
proximal of which were then subdivided into leading and trailing edge regions
(which lie dorsoventrally when the wings are folded) to give a total of
nine wing regions for stimulation (see Fig.
6). A single bin was stimulated using a fine paintbrush in all ten
animals sequentially, before a second bin was tested. Stimulus locations were
tested in a pseudo-random sequence. When all bins had been stimulated once in
all animals, the procedure was repeated another four times to give a total of
N=450 stimulations. The start positions were then changed and the
full stimulation protocol repeated (to give a total of N=900
stimulations). No individual animal was stimulated twice within 5 min. Half of
the animals were initially tested in the anterior start position whereas the
other half began in the posterior start position. We ensured that animals were
standing still when the stimulus was given. Spontaneous scratching did not
occur during an experiment in our setup. Behaviour was scored as either an
ipsilateral or contralateral scratch (in accordance with behaviour described
in Matheson, 1997
,
1998
) or as `no scratch'.
Since each animal was stimulated 5 times in each region (for each start
position), the occurrence of a single scratch yielded a response probability
of 20%. The likelihood of scratching therefore falls into six percentage
categories (0%, 20%, 40%, 60%, 80%, 100%). Non-parametric
(KruskalWallis) analyses of these data were carried out using SPSS
version 10 for Windows (SPSS Inc.) Data are presented as box plots in which
coloured boxes represent the interquartile range and the bold line in each is
the median value. Whiskers represent the full range of the data.
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In a third stimulation experiment to test the effectiveness of
chemoreceptive sensilla in eliciting scratching, five different animals were
set up without a start pole, so they stood with all of their tarsi on the foam
ball. They were placed in a fume hood. A point half way along the wing of each
animal was stimulated with a standard 0.2 ml puff of air delivered by hand
through a blunt 21-gauge needle attached to a 1 ml syringe. In a second round
of stimulations, the ipsilateral tarsus was stimulated in the same way. These
two stimuli were alternated until each animal had experienced five
stimulations of each site. The entire stimulation protocol was then repeated
using 0.2 ml of acetic acid vapour drawn from the headspace of a flask
containing glacial acetic acid (Rogers et
al., 2003), delivered in the same way. Leg movements made in
response to stimulation by either air or acetic acid vapour were scored as a
scratch, an avoidance response or as a nil response. To prevent sensitisation
or adaptation no animal was stimulated at any location more than once within 1
min.
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Results |
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Categories of trichoid hair
Hairs on the dorsal surface of the forewings fell into a clear trimodal
distribution of lengths (Fig.
1A) and were thus classified into three types, which could also be
distinguished on morphological and physiological grounds, as described
below.
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Short hairs ranged in length from 1446 µm (N=16 hairs;
Fig. 1B,C). Each was set in a
socket and stood perpendicular to the cuticle, with little curvature of the
shaft. The short hairs had a pore at the tip
(Fig. 1C) and were always
multiply innervated (Fig. 2A).
One of the sensory afferents in each sensillum responded to the initial
mechanical stimulus of an electrode being placed over the hair shaft, or
movements of the sensillum (Fig.
2A, lower trace), whereas one or more other afferents responded to
the solution contained within the recording electrode
(Fig. 2A, upper trace). These
hairs are therefore basiconic sensilla
(Kendall, 1970;
Newland, 1998
). We found no
hairs of less than 14 µm on the dorsal surface of the forewings using
either nailpolish casts or scanning electron microscopy. Basiconic sensilla
were only found on the dorsal surface of the forewings
(Fig. 2A) and the ventral
surface of the hindwings (Fig.
2E), and were not found on the ventral surface of the forewings or
the dorsal surface of the hindwings (Fig.
2). This distribution was consistent across all five animals
examined.
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Medium length trichoid hairs ranged from 73159 µm in length on the upper surface of the forewings (N=17) and inserted into sockets that had a raised rim (Fig. 1D). Their shafts had slight curvature and tapered evenly from base to tip. Medium length hairs were found on dorsal and ventral surfaces of both forewings and hindwings, and were always singly innervated (Fig. 2C,D,F). Neither medium nor long hairs possessed a pore at the tip of the hair shaft so we could not obtain tip recordings from intact hairs. Recordings were always obtained from the cut shaft.
Long hairs ranged in length from 316511 µm in 13 hairs and inserted into sockets that resembled those of the medium length hairs (Fig. 1F). Recordings revealed spikes of just one amplitude, elicited in response to movement of the hair shaft (Fig. 2B).
In addition to innervated hairs, the hindwing possesses many other hair-like structures on the wing veins and on the membrane of the anal region (Fig. 1G). They are of variable length and do not have a socket (Fig. 1H). The proximal 10-15mm of both the forewings and hindwings, near their articulation with the thorax, are also densely covered with longer hair-like structures (Fig. 1I). These also do not have a socket or a pore at the tip (Fig. 1J) and we could never obtain recordings from the intact or cut shafts on either wing. They appeared less stiff than tactile hairs, so that mechanical stimuli bent the shaft rather than pivoting the hair about its base.
Locations of trichoid hairs on the dorsal surface of the forewings
The overall ratio of basiconic:medium:long hairs on the dorsal surface of
the forewings was 4.8:2.0:1 in males and 3:2:1 in females. Basiconic sensilla
were distributed on many principal and cross veins on the dorsal surface of
the forewing (Fig. 3B,C). They
were most densely packed on the costa and subcosta, which together possessed
49±2.7% (mean ± S.E.M.,
N=10) of the total number on the dorsal surface of the wing (males
and females pooled). Only 8±2% were found on the postcubitus. The wings
of male and female locusts differ in size, so comparisons between the sexes
were based on the density of hairs rather than the absolute number. Across the
whole wing surface, there was no significant difference in the density of
basiconic sensilla between males and females (MANOVA,
F(1,56)=1.07, P=0.31) although there were
differences between all the individual veins (MANOVA, interaction
F(6,56)=27.8, P=0, see
Fig. 4A).
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Medium length hairs were unevenly spaced on the costa, subcosta, radius and media (Fig. 3B,C). 88±5.2% of medium length hairs were found on the subcosta alone, with all other veins having lower densities (MANOVA, F(6,56)=83.5, P<0.01). The spacing and orientation of medium length hairs on the subcosta are illustrated in Fig. 1E. They generally pointed towards either the leading or trailing edge of the wing. Females had a 1.5-fold greater density of medium length hairs on the subcosta (14.9±1.1 hairs cm1) than did males (9.7±1.7 hairs cm1: ANOVA, F(1,8)=6.32, P<0.05, see Fig. 4B). Medium length hairs were more sparsely distributed on the ventral surface of the forewing, and on both surfaces of the hindwing.
Long hairs had the most restricted distribution, with 93±3.6% occurring on the postcubitus. An additional cluster of hairs beyond the distal end of this vein were counted as wingtip hairs (Fig. 3B,C). Females had a 1.5-fold greater density of long hairs on the dorsal forewing postcubitus (8.1±0.2 hairs cm1) than did males (5.3±0.5 hairs cm1: MANOVA, F(1,56)=29.37, P<0.01). This difference increased to twofold if hairs at the distal end of the postcubitus were included; see Fig. 4C).
When the forewing was extended laterally, as occurs during flight, the long hairs lay slanted towards the trailing edge of the wing. At rest, however, the wings are folded along the claval furrow, with the vannus of one forewing overlapping the other. The long hairs then stand up vertically so that they protrude above the animal (Fig. 5). In this position, the postcubitus veins of the two forewings present two parallel rows of long hairs along much of the length of the wings (Fig. 5B,C).
To relate the distribution of hairs to the probability of eliciting scratching behaviour, we recounted the number of hairs in each of the nine regions used as stimulus sites in the behavioural analyses (Fig. 6C, and see Materials and methods).
The number of long hairs were evenly spaced, therefore the number of hairs per region did not differ significantly along the proximaldistal axis in trailing edge regions 14 (Fig. 6A, ANOVA, F(3,36)=0.35, P=0.79).
The number of medium hairs per region differed significantly along the wing from regions 69 (Fig. 6B, ANOVA, F(3,36)=4.30, P<0.05). The greatest number was in region 8 in both males (containing 35±2.1% of the total number of medium length hairs) and females (40±2.6%). The difference in the number of medium hairs between males and females also differed significantly along the length of the subcosta (ANOVA, F(3,32)=3.51, P<0.05). The largest difference between the two sexes occurred in region 7, where females had a total of 26.2±2.1 and males 8.2±1.5 medium length hairs, which is a 3.2-fold difference between the sexes.
Probability of eliciting a scratch
Effect of gender
When standing in the anterior start position, females scratched
ipsilaterally (scratch of the ipsilateral wing with the ipsilateral leg) in
response to 60% of stimuli (interquartile range: 60%), whereas males scratched
ipsilaterally in response to only 20% of stimuli (interquartile range: 60%).
This difference is significant (KruskalWallis test,
2=7.48, d.f. 1, P=0.006).
Effect of stimulus site
When standing in the anterior start position, the likelihood of eliciting a
scratch differed significantly for stimuli applied to different regions of the
forewing surface (Fig. 7,
KruskalWallis test, 2=24.51, P=0.002).
Stimulation of trailing edge regions was most successful at eliciting
scratching (Fig. 7A).
Stimulation of these sites elicited a scratch on 20% of occasions (median,
interquartile range 20%), whereas stimulation of leading edge regions
(Fig. 7B) gave rise to a median
likelihood of 0% (interquartile range 20%), both sexes pooled
(KruskalWallis test,
2=20.95, d.f. 1,
P=0.000). There was no significant difference in the scratching
probability of either sex along the anterio-posterior axis of the trailing
edge regions 14 (males, KruskalWallis test,
2=0.37, d.f. 3, P=0.78; females, KruskalWallis
test,
2=0.63, d.f. 3, P=0.61) or leading edge regions
69 (males, KruskalWallis test,
2=0.50, d.f. 3,
P=0.56; females, KruskalWallis test,
2=0.72,
d.f. 3, P=0.56).
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Likelihood of eliciting a contralateral scratch
When standing in the anterior start position, stimulation of trailing edge
regions was significantly less likely to elicit a contralateral scratch
(scratch of the contralateral wing with the contralateral leg) than was
stimulation of leading edge regions (KruskalWallis test,
2=22.0, d.f. 1, P=0.000). Females scratched
contralaterally in response to 20% of stimuli (interquartile range: 45%),
whereas males scratched contralaterally in response to only 0% of stimuli
(interquartile range: 20%) when data were summed across all wing regions
(KruskalWallis test,
2=4.81, d.f. 1,
P=0.028).
Effect of hind leg start position
To determine the effect of start position we first pooled data from the two
sexes. Start position had a significant effect on the overall likelihood that
a touch on a wing elicited an ipsilateral scratch (KruskalWallis test,
2=3.86, P=0.049). Locusts standing in the anterior
start position (see Fig. 7C)
had a 20% overall likelihood of scratching (median, interquartile range: 40%)
whereas those standing in the posterior start position had a 0% overall median
likelihood (interquartile range: 20%).
When the animal was standing in the posterior start position, females
scratched ipsilaterally in response to 20% of stimuli (interquartile range:
20%), whereas males scratched ipsilaterally in response to 0% of stimuli
(interquartile range: 25%). This was not significant (KruskalWallis
test, 2=0.23, d.f. 1, P=0.630). Because of the low
overall likelihood of eliciting scratches when animals stood in the posterior
start position, we could not carry out a detailed analysis of the effect of
stimulus site. Nevertheless, there was an overall effect of stimulus site
(KruskalWallis test,
2=17.05, d.f. 6,
P=0.030), and the pattern of scratch probability across regions was
similar to that for the anterior start position shown in
Fig. 7 (data not shown).
Relationships between numbers of hairs and probability of eliciting a scratch
When data for both sexes were pooled there was a significant correlation
between the number of medium length hairs in a region and the probability that
stimulation of that region would elicit an ipsilateral scratch (Spearman's
rank correlation test, =0.307, P=0.027). When the sexes were
analysed separately, there was no significant correlation between number of
medium length hairs in a region and the probability of eliciting a scratch
(Pearson's test, males:
=0.112, P=0.43; females:
=0.410, P=0.25). This lack of significance will in part
be due to the low inter-animal variability in the number of hairs and the
coarseness of the probability scale.
Due to uniform number of hairs per region (see `Locations of trichoid hairs' above), there was no correlation between the number of long hairs in a region and the probability of eliciting an ipsilateral scratch (Pearson's correlation, r=0.220, P=0.173).
Ablation of exteroceptors
Ablation of long hairs on the postcubitus vein (which runs through trailing
edge regions 14) had three main effects. First, it almost completely
abolished responsiveness to touch in regions 14 in all animals
(Fig. 8A), and therefore
significantly reduced the overall probability of eliciting an ipsilateral
scratch (KruskalWallis test, 2=12.15, d.f. 1,
P=0.000, both sexes pooled). Second, there was an increase in the
sensitivity of leading edge regions 69
(Fig. 8B) and the wing tip
region 5 (Fig. 8A)
(KruskalWallis test,
2=28.21, d.f. 1,
P=0.000). Third, it significantly affected the likelihood of
contralateral scratching (KruskalWallis test,
2=14.70,
d.f. 1, P=0.000). In control stimulations, contralateral scratching
occurred more often in response to stimulation of leading edge regions than
trailing edge ones. But following the ablation of hairs on the postcubitus,
the probability of a contralateral response to stimulation of non-manipulated
leading edge sites was reduced from 40% to 0% (interquartile range 40%). The
probability of eliciting a contralateral scratch by stimulation of trailing
edge regions 14 was not affected by ablation since median probability
was 0% both before and after (interquartile range 40%).
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Chemical odour stimulation of exteroceptors
Puffing the odour of acetic acid over the dorsal surface of a forewing was
no more likely to elicit an ipsilateral scratch than was air
(KruskalWallis test, 2=1.48, d.f. 1, P=0.22)
(Table 1). In contrast, puffing
the odour of acetic acid over the tarsus of a hind leg was more likely to
elicit an avoidance response of that leg than was an air-puff applied to the
tarsus (KruskalWallis test,
2=50.20, d.f. 1,
P=0.000) (Table
1).
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Puffing the odour of acetic acid over the tarsus of a hind leg was sevenfold more likely to elicit an ipsilateral hindleg avoidance response than was odour stimulation of the forewing likely to elicit an ipsilateral scratch (Table 1).
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Discussion |
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Distribution of exteroceptors
The lengths of basiconic sensilla on the wings of the locust are similar to
the range of lengths of basiconic sensilla on the hindleg tibiae (1446
µm) (Burrows and Newland,
1994). They occur on all veins across the whole dorsal surface of
the locust forewing, but not on the membrane between veins and cross veins.
Female locusts have more basiconic sensilla on their forewings than do males,
but also have larger wings; therefore the receptor density is the same in the
two sexes. Basiconic sensilla are present only on the dorsal surface of the
forewings and the ventral surface of the hindwings. This pattern of
distribution makes sense for contact chemoreceptors, since the dorsal surfaces
of the forewings are permanently exposed to the environment, whereas the
ventral surfaces and the hindwings are protected at rest
(Uvarov, 1966
).
The comparative studies of Zahwilichowski in the 1930s described
many multiply innervated sensilla, but such receptors were not recognised as
being chemoreceptors (basiconic sensilla) (Za
hwilichowski, 1934a,b,
1936). In locusts too, multiply innervated hairs of approximately 40 µm in
length were described (Knyazeva, 1934,
1970
), but again were not
shown to be chemosensory. Few studies have explicitly recognised the presence
and location of chemoreceptors on the insect wing (Angioy, 1981; Pietra, 1980;
Dickinson, 1997).
Hairs longer than 40 µm have not previously been described on the
surface of locust forewings (Knyazeva,
1970). We can find no report of hairs longer than 200 µm on the
forewing surface of any orthopteran species, although such long hairs are
found on the wing's articulation with the thorax
(Knyazeva, 1970
). Trichoid
hairs on the hindlegs range from 60780 µm
(Newland, 1991
) and there are
long filiform hairs on the prosternum (500600 µm;
Pflüger and Tautz, 1982
),
head (up to 300 µm; Weis-Fogh,
1949
) and cerci (20500 µm;
Thomas, 1965
).
We show that the distributions of medium (73159 µm) and long (316511 µm) hairs on the forewings of Schistocerca gregaria are very similar to that described for the shorter hairs on the forewing of the grasshopper Melanoplus sanguinipes (Albert, 1976). In both cases the longest hairs (approximately 100 µm in M. sanguinipes) are restricted to the vein delineating the trailing edge, whereas the medium length hairs are most numerous on the veins supporting the leading edge. Note that the key figure (fig. 26) in Albert (1976) incorrectly labels the orientation of the wing, and mislabels the veins. Long hairs are far less numerous on the locust forewing than are medium length or short hairs, but the reverse is true of M. sanguinipes. Overall M. sanguinipes has many more tactile hairs than Schistocerca gregaria, even though it is approximately half the size.
Locust forewings have far fewer long and medium length hairs than do the larger hindwings. On a single hindwing there are approximately 12 400 hairs and bristles, 1160 of which are on the principal veins (Altman, 1978). Many of the hair-like structures lying on the membranous anal region of the hindwing are not innervated.
Scratching probability and tactile hair densities
The overall probability of eliciting scratching behaviour by touching a
small region of a forewing is low. Using stimuli that cover a larger region,
or that last for longer, can increase the probability (data not shown). For
foreleg grooming of the sternum, isolation of the prothoracic ganglion
increases the likelihood of eliciting the behaviour from virtually 0% to over
95% likelihood (Rowell,
1969).
Stimulating trailing edge regions of a forewing is significantly more likely to elicit scratching behaviour than is stimulation of leading edge regions. The principal vein present in this area is the postcubitus, which is covered in regularly spaced, long tactile hairs. Each of the four trailing edge regions (14) contains the same number of long hairs, and locusts are equally likely to scratch in response to stimulation of any of them.
In the leading edge regions 69, most hairs occur on the subcosta. They are all short or medium length hairs. Across the sexes, there is a correlation between the number of medium length hairs per region and the probability of eliciting a scratch. The small variation in the number of hairs per region and the relative coarseness of the probability scale (five probability bins) meant that we could not demonstrate whether this correlation also holds within each sex.
The position of the ipsilateral hindleg at the start of stimulation also
has a significant effect on the overall likelihood of scratching in response
to stimulation of the forewing's dorsal surface. This suggests that
proprioceptive inputs signalling the posture of the hindleg must impinge onto
the local neuronal circuits that generate the aimed scratching movements. Such
convergence of hindleg proprioceptive inputs and forewing exteroceptive inputs
onto local and intersegmental interneurones has been demonstrated by Matheson
(2002), providing the
opportunity now to analyse how these two types of sensory information interact
in the generation of an aimed movement.
Gender-specific differences
The forewings of female locusts have more medium length hairs on the
subcosta, and more long hairs on the postcubitus, than do those of male
locusts, and these differences are greater than predicted by the difference in
wing size. In contrast most sexual dimorphisms in sensilla numbers observed in
other insects species are related to differences in body size
(Chapman, 1982). Exceptions to
this rule occur mainly on the antennae of species that demonstrate
sex-specific differences in feeding habits or pheromone detection
(Chapman, 1982
; Linardi and
Chiarini-Garcia, 2002). Sexual dimorphism in hair numbers has not previously
been described in locusts. The sexual dimorphism that we describe is
positively correlated with the likelihood of eliciting a scratch (see previous
section). Solitarious phase locusts have more olfactory sensilla on their
antennae and more mechanosensory sensilla on their legs than do gregarious
phase animals and these differences may be related to differences in the
behaviours of solitarious and gregarious animals
(Greenwood and Chapman, 1984
;
Ochieng, 1998; Rogers et al., 2000). Solitarious locusts groom spontaneously
less frequently than do gregarious locusts
(Simpson et al., 1999
), but
there has been no systematic study of either wing hair distributions or the
strengths of sensory synapses in the two phases. Rearing conditions can also
affect receptor numbers in locusts (Rogers
and Simpson, 1997
), but this could not have contributed to the
differences that we describe, as all the locusts were reared together. The
gender-specific difference in sensilla number is consistent with the
difference in the probability with which a stimulus elicits a scratch. In the
trailing edge regions where females possess twice as many long hairs as do
males, females are 1.5-fold more likely to scratch in response to tactile hair
stimulation. It is not known if the form of a scratching movement differs
between males and females (Dürr and
Matheson, 2003
), but the difference in hair density raises the
possibility that females could aim their movements more precisely if the
target is encoded in a more finely grained sensory representation.
Function of exteroceptors
Mechanosensory afferents from basiconic sensilla on the legs are more
sensitive to touch than are those of tactile hairs, and they are therefore
effective at signalling very close contact with food, obstacles or
conspecifics (Newland and Burrows,
1994; Rogers and Newland, 2003). Individual basiconic sensilla on
the hindleg tibia are capable of eliciting spikes in spiking local
interneurones (Burrows and Newland,
1994
). Basiconic sensilla on the fore- and hindwings presumably
enable the animal to respond to both mechanical stimuli and to chemicals
brought into contact with the wing cuticle. These sensilla are the most
numerous of the three hair types on the forewing dorsal surface and must
represent an important form of mechanosensory input from the wing surface. The
highest densities of basiconic sensilla are on the subcosta and costa, but
mechanical stimulation of these leading edge regions has a lower probability
of eliciting a scratch than stimulating the trailing edge regions where
basiconic sensilla are sparsely distributed. We conclude that the
mechanosensory afferents of basiconic sensilla have a weaker input to the
networks underlying scratching than do those of the long hair afferents.
Both mechanosensory and chemosensory afferents from basiconic sensilla on
the mesothoracic leg project somatotopically within the mesothoracic ganglion
(Newland et al., 2000). Their
projections overlap considerably with the arborisations of mechanosensory
afferents from tactile hairs on corresponding regions of the leg
(Burrows and Newland, 1994
),
suggesting that chemosensory information might be processed together with
mechanosensory information within the CNS. Stimulation of basiconic sensilla
on the forewing with a weak solution of acetic acid can elicit a reliable
hindleg targeted scratching movement (K.P., personal observation). The odour
of acetic acid alone can elicit `leg-waving' behaviour in grasshoppers
(Slifer, 1954
;
Slifer and Finlayson, 1956
;
White and Chapman, 1990
) and a
leg avoidance reflex in locusts (Newland,
1998
). In contrast to this stimulation of the tarsus, acetic acid
odour puffed over a forewing is no more successful at eliciting a scratch than
is a puff of air. This may result from a higher threshold of response for wing
chemoreceptors compared to leg chemoreceptors, or may indicate a more
fundamental difference in the way that the information from the two surfaces
is processed.
Ablating the long trichoid hairs on the postcubitus vein of a forewing
reduces the high sensitivity of the trailing edge regions through which this
vein runs. This manipulation also removed the few basiconic sensilla on this
vein although all others, including those on the nearby cross veins, remained
intact. The striking reduction in responsiveness of trailing edge regions
following hair ablation clearly points to a role of the long hairs in
eliciting a scratch. These hairs are the least numerous of the three types,
and yet are highly effective at eliciting scratching behaviour. At rest, the
dorsal position of the long hairs, combined with their vertical orientation,
make them well suited to detecting predators or conspecifics approaching from
above. This may be particularly relevant to female locusts, since these hairs
would be deflected by the thorax and abdomen of male locusts during both the
precopulatory passive phase and copulation, which can last for several hours
(Uvarov, 1966,
Parker et al., 1974
).
Stimulation of regions that do not contain long hairs can also elicit aimed
scratching, albeit with a lower likelihood. Basiconic sensilla and medium
length hair sensilla presumably contribute to this drive. All hair types,
therefore, could be stimulated by the presence of foreign material or
parasites on the wing, which may be removed by scratching.
Our findings suggest that mechanosensory afferents from hairs on the
forewings (which are mesothoracic appendages) provide an important input to
metathoracic networks that drive hindleg scratching (Berkowitz and Laurent,
1996a,b
;
Matheson, 1997
). In this
context, forewing hairs function much like tactile hairs on the legs,
stimulation of which can initiate local leg reflexes in which the hindleg is
lifted away from the site of stimulation by the coordinated action of several
leg joints (Burrows, 1996
).
These leg avoidance reflexes are computed locally, and involve movement of the
stimulated appendage, whereas scratching movements made in response to
stimulation of forewing hairs are computed intersegmentally. Scratches involve
movement of one appendage (the hind leg) towards a target on another appendage
(the wing) in a cyclical and often repetitious movement, which can outlast the
duration of the stimulus. When the stimulus is prolonged or moves along the
wing, locusts re-aim their leg movements appropriately
(Matheson, 1998
), indicating
that forewing tactile hairs provide continuous feedback throughout the
movement. Whether leg hairs that trigger leg avoidance reflexes can also
provide ongoing feedback to modify those movements is unknown.
Scratches that are aimed at different locations on a wing necessarily
differ in detail from one another, but there is no evidence that different
forms of scratching are used to reach different locations on the forewing, and
the behavioural responses thus form a continuum
(Dürr and Matheson,
2003). Leg reflexes, in contrast, fall into discrete categories
depending on the region of the hindleg being stimulated, and these categories
can be related to distinct boundaries between the receptive fields of
interneurones that receive inputs from the tactile hair afferents (Siegler,
1986). For scratching movements, hindleg proprioceptive inputs modulate both
the initial outward trajectory and the overall accuracy
(Dürr and Matheson,
2003
). We show that the overall probability of eliciting a scratch
differs for different start positions, so leg proprioceptive inputs may also
modulate the overall gain of wing mechanosensory pathways. Moreover, since the
kinematics of a scratch depend on start position
(Dürr and Matheson,
2003
), it is likely that the effective somatosensory receptive
fields of interneurones and motor neurones driving scratching are modulated by
leg proprioceptive inputs. At least one class of metathoracic local
interneurone is strongly excited by both wing exteroceptive inputs and hind
leg proprioceptive inputs (Matheson,
2002
), but the detailed interactions between the two modalities
within such neurones remain to be elucidated.
Previous papers describing wing tactile hairs have proposed that they are
directional detectors of air pressure or wind velocity during flight
(Knyazeva, 1970; Albert, 1976;
Altman, 1978), but there is no direct evidence for such roles. Recordings of
hindwing nerve 1A during flight reveal that many neurones fire in response to
wing movements, but many of these are afferents from campaniform sensilla and
it is not known if any of the remainder are afferents from tactile hairs
(Wilson, 1961
; Gettrup,
1965
,
1966
). We have shown that
locust forewing hairs respond to chemical and mechanical stimuli when the
locust is at rest and are responsible for eliciting hindleg scratching
movements.
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