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First published online October 18, 2006
Journal of Experimental Biology 209, 4363-4370 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02485
Ontogeny of air-motion sensing in cricket
1 Université de Tours, IRBI UMR CNRS 6035, Parc Grandmont, 37200
Tours, France
2 IRD (R072), c/o CNRS LEGS, BP1, 91198 Gif-sur-Yvette cedex,
France
* Author for correspondence (e-mail: jerome.casas{at}univ-tours.fr)
Accepted 10 August 2006
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Summary |
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Key words: European wood cricket, functional morphology, mechanoreception, population coding model, sensory development
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TOPSummaryIntroductionMaterial and methodsResultsDiscussionReferences |
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). Given that
resource consumption and predation risk are generally related to body size,
many species undergo significant shifts in food or habitat use as they grow
(Werner and Gilliam, 1984;
Heming, 2003) and show
substantial commensurate developmental adjustment of their sensory equipment.
Shift in sensitivity and signal coding during ontogeny has been recorded in a
variety of taxa and senses including anuran and fish vision
(Jaeger and Hailman, 1976;
Job and Shand, 2001), mammal
olfaction (Doty et al., 1984),
mammal and fish hearing (Rubel,
1984; Kenyon,
1996) and fish electroreception
(Denizot et al., 1998). In
particular, sensors involved in the detection of predators represent
interesting models in which to examine the functional consequences of change
in sensory morphology during development. Juvenile stages generally suffer
high rates of predation and their sensory systems, although often reduced,
must provide the necessary information about the approaching predator to judge
whether to respond and at what moment. Thus, ontogenetic changes in sensory
morphology may be expected to have important consequences for susceptibility
to predatory attack and, hence, survival.
Among anti-predator sensory systems, the air-current-sensitive cercal
system of orthopteroids (cricket and cockroaches) is one of the most sensitive
in the animal kingdom (Shimozawa et al.,
2003). These insects bear on their cerci hundreds of
mechanoreceptive filiform hairs that respond to the faintest air movements,
down to 0.03 mm s-1 (Shimozawa
et al., 2003). Hair deflection produces a mechanical stress in the
cercal afferent neuron under the hair base. The extreme sensitivity of the
cricket's wind-detecting system allows the use of air flow patterns for early
detection of flying predators, even at relatively large distances [up to 30
times their body length (Gnatzy and
Heußlein, 1986)]. The hundreds of filiform hairs of varying
lengths composing the cercal array of hairs and their associated neurons can
encode the acceleration, the frequency and the direction of predatory air
signals, providing the necessary information for the cricket to escape
efficiently. Although a substantial amount of knowledge has accumulated on the
physiology, the neurobiology and the biomechanics of this sensory system in
adults (e.g. Camhi, 1984;
Gnatzy, 1996;
Shimozawa et al., 2003), the
morphological and functional aspects of air sensing have not been as well
studied for earlier life history stages. Because most predation events do
occur in early instars (Dangles et al.,
2006a), studies that focus on juveniles are crucial to better
understand the ecological significance of wind sensors throughout the
development of these insects.
Events leading up to the development of sensory function include the
simultaneous maturation of many neural and mechanical properties. In crickets,
the increase in hair length during postembryonic development generates changes
in coding properties of air velocity and acceleration by afferent neurons
(Chiba et al., 1988). By
contrast, the biomechanics of filiform hairs shows no clear changes either in
terms of threshold angles or oscillation properties
(Kanou et al., 1988;
Kämper, 1992). More
obviously, the cercal system of crickets undergoes important changes in number
and length of filiform hairs as the cricket grows
(Kanou et al., 1988) (O.D.,
personal observations). Surprisingly, no studies have ever quantified these
changes and few have investigated the implications for cricket sensitivity to
air currents (e.g. Chiba et al.,
1988). The aim of the present study is to document how air current
sensitivity changes as the full complement of receptors develops. We first
quantified, precisely and exhaustively, changes in number, length and spatial
arrangement of hairs over the surface of the cercus as a cricket grows.
Second, we investigated the functional implications of these morphological
changes by modelling the tuning efficiency of each instar submitted to
biologically relevant oscillatory air signals by natural predators.
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Material and methods |
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). The wood
cricket life cycle consists of one generation every second year with diapause
in both eggs and juveniles stage during winter
(Gabbutt, 1959b). Their
development comprises eight larval instars and one adult instar. The larval
development begins in June and early July with the first instar and successive
instars occur until November when the insect over-winters as the fifth or
occasionally the sixth instar. Growth starts again the following March and the
sixth, seventh and eighth instars are present in the following two months
until the adults finally appear in June or July
(Gabbutt, 1959b).
Cricket sampling
Juvenile and adult male and female wood crickets were collected from ground
litter on several occasions (spring, summer and autumn 2004) in a mixed
deciduous forest nearby Tours (Larçay forest,
49°01'50''N, 06°05'52''E). Crickets were placed
in 70° alcohol and returned to the laboratory. Following the method of
Campan (Campan, 1965), instars
were determined by measuring the tibia length of the posterior legs using a
micrometer mounted on a stereomicroscope (Leica, MZ 13, Wetzlar, Germany).
Seven instars out of nine were selected for this study: instar I, II, III, V,
VI, VII and adult (Ad).
Cercus scanning
The hair array structure was examined by scanning electron microscopy (SEM,
DSM 982 GEMINI, LEO Microscopie, Cambridge, England) of cerci that had been
dissected from crickets, dehydrated and sputter coated with platinum. To
perform a complete survey of wind sensitive hairs inserted on the
three-dimensional conical surface of the cercus (see
Fig. 1), we built a rotating
stage which allowed us to take images from different angles under the
microscope. For each instar, we took a set of five SEM images, from the base
to the tip of the cercus, at eight different angles (0°, 45°, 90°,
135°, 180°, 225°, 270° and 315°). Ten additional images at
lower magnification (x40) were taken to measure the length of long
filiform hairs (see below). In total, 50 SEM pictures were taken for each
instar, and for technical reasons, replication was performed for only three
instars (I, III, and Ad). We found weak inter-individual variability (<5%)
in the structure of the cercal hair array, confirming previous studies on the
cercal sensory system of crickets (Dangles
et al., 2005; Magal et al.,
2006). We observed no differences between left and right cerci
(O.D., F.V., D.P. and J.C., unpublished data).
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Morphological measurements on cerci
In addition to cercus length, three types of measurements were performed on
cercus images from each instar. First, we counted all filiform hairs and
calculated their overall density assuming that the cercus has a conical shape.
As complementary measurements, we also counted the number of two other types
of cercal receptors, the clavate and trichoid hairs, which are reported to be
involved in the perception of gravity and touch
(Edwards and Palka, 1974),
respectively (see Fig. 1).
Second, we calculated the three-dimensional coordinates of each filiform hair
over the cercus. These data about hair positioning allowed us to investigate
modifications in the spatial arrangement of receptors throughout cricket
development (see Statistical analyses). Third, we measured the base diameter
of each filiform hair on SEM pictures using Scion Image for Windows (Scion
Corporation, Frederick, MD, USA). The base diameter (d) allowed us to
estimate with precision the length of the hair (L) as there is an
allometric relationship, L=a.db, between these two
variables (Kumagai et al.,
1998; Magal et al.,
2006). We calculated a and b parameters for each
cricket instar, based on simultaneous measurements of base diameter and length
for a series of 40 hairs of varying lengths perfectly located in the image
plane.
Statistical analyses
We used the pair correlation function G(r)
(Ripley, 1981) to analyse the
arrangement of cercal filiform hairs for each cricket instars. Following
guidelines (Apanasovich et al.,
2003), the conical point pattern of hairs over the cercus was cut
lengthwise into two pieces corresponding to the lateral and the medial
surfaces of the cercus. Owing to the presence of aggregated clavate hairs the
basal part of the cercus was not considered for spatial analyses. The
distribution pattern (random, aggregated or regular) of filiform hairs was
evaluated by comparing the observed data with the null model of complete
spatial randomness (for details, see
Ripley, 1981). All spatial
analyses were performed using the `Spatial Stat' package of R software (R
Development Core Team).
Frequency distributions of hair length were decomposed into Gaussian
distributions using a combination of a Newton-type method and expectation
maximization algorithms. Mean (µn), variance
(
n), and proportion (
n), for each n
component distributions were calculated using the `mixture distribution'
package of R software (R Development Core Team). A 
2 function
was used for parameter estimations and goodness-of-fit testing when adjusting
curves to histograms.
Modelling the sensitivity response of crickets to air signals
We used a mathematical model (Magal et
al., 2006) to predict the consequences of ontogenetic changes in
the cercal hair array structure for cricket sensitivity to air signals. This
model combines the biomechanics of hair movement, the distribution of hair
length in the entire array, and the relationship between single hair movement
and its neurophysiological activity to predict the overall response of the
cercal array to air signals of various intensities and frequencies. Briefly,
an additive population coding of sinusoid signals of varying frequencies and
velocities, taking into account hair directionality, produced the cercal array
tuning curve. The proportions of each category of directionality were supposed
constant through development. The neurophysiological activity was implemented
using the relationship between frequency and triggering velocity threshold
values for each hair length (for details, see
Magal et al., 2006). Hair
number and the variation of hair length are key features of the cercal system
of crickets as they fractionate both the intensity and the frequency range of
an air stimulus. Longer hairs have their peak response at low frequency,
whereas shorter hairs have a flat response over most of the frequency range,
with a peak response at high frequency. The output of the model, the canopy
response (CR, in radians), is the sum of the maximal hair deflection in the
array of hairs.
In spite of the growth of filiform hairs throughout development, their
threshold angle remains unchanged for a given hair length
(Kanou et al., 1988). This
property allowed us to estimate theoretically the sensitivity of the cercal
array during cricket development by implementing the model with the hair
length distributions measured for each cricket instar. We thereby obtained for
each instar the cercal canopy response as a function of frequency (0-300 Hz)
and intensity (0.05-5.0 cm s-1) of biologically relevant
oscillatory air signals from natural predators (see
Gnatzy, 1996;
Dangles et al., 2005).
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Not only are more filiform hairs added to the surface of cerci during each
successive moult of the cricket but existing filiform hairs increase in
length. In the first instar, the hairs vary in length from 33 µm to 407
µm and their length distribution presents a unimodal normal shape with a
mean value of 191 µm and a variance of 113 µm
(Fig. 3,
Table 1). A bimodality of the
hair length distribution appears from the second instar onwards, clearly
separating hairs into two populations of different lengths
(Fig. 3). Whereas the mean of
short hair populations is relatively constant throughout development
(µ1=142±34), the mean of long hair population
progressively shifts to larger values through each instar
(µ2=504 µm in instar II to 730 µm in adult,
Table 1). This increase in
µ2 is accompanied by an increase in 2
(2=90 µm in instar II to 172 µm in adult), as a result
of an increase in maximal length of hairs as the cricket develops (from 710
µm in instar II to 1100 µm in adults,
Fig. 3). Interestingly, the
proportions of short (
1) and long hairs (2) are
constant during the development from instar II onwards, around 0.80 and 0.20,
respectively (Table 1).
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Discussion |
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TOPSummaryIntroductionMaterial and methodsResultsDiscussionReferences |
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); vision in fish
(Higgs and Fuiman, 1996)],
newly hatched crickets have already a developed air-sensing system. Sixty
filiform hairs of varying length compose the array of each cercus of the first
instar of N. sylvestris, a number comparable to that observed in
other cricket species [e.g. 56 in Acheta domestica
(Kämper, 1992)]. Our
model suggests that the cercal system is fully functional at this instar,
capable of responding to wide array of frequencies as was experimentally shown
by Kämper (Kämper,
1992) on early instars of A. domestica. The model also
suggests that the development of optimal air-sensing acuity is fairly linear
in crickets. Here again, this would contrast with other sensory systems such
as visual, auditory and somatosensory systems in mammals in which there is a
variation in the rate of sensory function throughout development (e.g.
Berardi et al., 2000).
A surprising result of our study was the linear decrease in cercal filiform
hair density throughout cricket development: whereas the increase in new
filiform hairs after each moult is logarithmic, the cercal surface increases
exponentially (result not shown). Two main mechanisms may explain why filiform
hair increase does not follow that of cercus surface. First, other types of
receptors (clavate and trichoid hairs) are inserted on the cercus as cricket
grows, thus limiting the surface available to insert new filiform hairs.
Second, as crickets produce longer filiform hairs after each moult, it seems
that a minimal distance (40-50 µm) has to be conserved between neighbour
hairs, potentially to avoid interference during oscillation (see
Bathellier et al., 2005). Our
spatial analyses indeed confirmed that a regular distribution of filiform hair
array takes place as crickets develop.
It was also intriguing for us to find that the cercal array organisation in
first instar cricket is very different from that of cockroach (Periplaneta
americana) despite evident biomechanical, physiological and neurological
similarities between the two systems
(Camhi, 1984). Cockroach bears
only two wind-sensitive hairs on each cercus after hatching
(Camhi, 1984). Because both
first-instar crickets and cockroaches have been observed to efficiently escape
from predator as a result of these stimuli
(Kämper, 1992) (O.D. and
D.P., personal observation), the question arises as to what extent hair number
affects perception and behaviour of these animals. We suppose that the benefit
of having more hairs allows the detection of a wider range of signals of
different types and from different directions. More generally, this
dissimilarity between cricket and cockroach hair equipment underlines the fact
that a specific sensory function may develop differently among related
species. This has been reported, for example, within the group of electric
fish in which Mormyrids are the only members to possess a complete larval
electric system (Denizot et al.,
1998).
Development of the bimodal length-frequency distribution of the cercal hair array
The major finding of this study is that the bimodality in hair length,
underlying air-sensing function in adult crickets, is a result of changes that
occur during development. Length is indeed an essential parameter of filiform
hairs because the moment of inertia and the total deflecting torque applied
from the air vary with length (Shimozawa
and Kanou, 1984). As previously reported
(Magal et al., 2006), this
bimodal distribution can explain the difference in frequency tuning of various
frequencies as a function of signal intensity
(Fig. 5A,B). At small air flow
velocity (0.05 cm s-1), crickets detect faint air movements through
their long and sensitive hairs on the one hand and through a few short hairs
reacting near their resonance frequencies on the other hand. As air flow
velocity increases (5 cm s-1) the overriding contribution of short
hairs vibrating below their best frequencies produces a downward tuning shift
to lower frequencies. This explains why the peak frequency of the first instar
is located at higher frequency, as there are no long hairs and hence a lack of
bimodality.
Another characteristic of the bimodal length-frequency distribution throughout cricket development is that, after the first moult, the proportions of short and long hairs remain constant (0.8 versus 0.2, respectively). As a functional consequence, the best-tuned frequency remains fairly constant throughout cricket development, between 150 and 180 Hz. This suggests that the development of the cricket cercal system is made of change and constancy: although changes in the number of hairs increase the overall sensitivity of adult crickets the value of the best tuned frequency is fixed after the second instar. Further experimental data on the evolution of hair biomechanical properties during the course of wood cricket development would be useful to refine the predictions of our model.
Ecological significance of air-sensing development in crickets
Several works have laid the hypothesis that the timing and priority of
morphological changes throughout development are linked to functional demands
and ecological requirements. For example, Jaeger and Hailman
(Jaeger and Hailman, 1976)
proposed that a shift to midspectrum (green) preference in laboratory
phototactic tests of young tadpoles may be ecologically adaptive, in that it
directs larvae to green plants that provide food or shelter. Similarly,
ontogenetic shifts in the spectral sensitivity of cone photoreceptors observed
in juvenile teleosts have been associated with changes in either habitat or
diet (Shand et al., 1988;
Novales Flamarique, 2000). In
crickets, one can hypothesize that changes in the sensitivity to air signals
may have consequences for predator detection during life cycle. Experimental
studies under both laboratory and field conditions have reported that wood
crickets can be preyed upon by flying predators at various instars
(Gnatzy, 1996;
Dangles et al., 2006a),
although little is known about their effect on population dynamics. For
instance, parasitoid wasps (Sphecidae) are known to be potential predators of
N. sylvestris (Gnatzy,
1996) and generate dominant acoustic frequencies around 150-200 Hz
(Tautz and Markl, 1978;
Gnatzy and Heußlein,
1986). When a cricket detects the oscillating signal emitted by a
flying wasp, it stops moving, therefore trying to avoid being spotted by the
wasp and to position itself for a violent kick response
(Gnatzy, 1996). Other
parasitoid predators such as Larinae (Hymenoptera) and Tachinidae (Diptera)
also predate on crickets (Menke,
1992; Walker,
1993) and have wing beat frequencies around 200 Hz
(Wigglesworth, 1972). Wood
crickets after the first moult, have been found to be best tuned to these
values, suggesting that the development of the cercal array of hairs may have
evolved in response to such signals. Moreover, from a physiological view
point, our results support recent estimates of cercal afferent neuronal
activity based on dejittered spike means, which indicate that stimulus
frequency selectivity in crickets extends to 
200 Hz with peak sensitivity
around 150 Hz (Aldworth et al.,
2005).
We also know that crickets are confronted with other types of close range,
non oscillating and low frequency signals emitted by running predators such as
Liris wasps (Gnatzy and
Kämper, 1990) or wolf spiders
(Dangles et al., 2006b), the
latter having an outstanding impact on cricket survival in early instars
(Dangles et al., 2006a). It is
now therefore mandatory to observe hair movement during the attack of running
predators, as the results from our simulations only strictly hold true for
oscillatory signals such as those emitted by flying predators.
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