Hearing in hooktip moths (Drepanidae: Lepidoptera)
1 Center for Sound Communication, Institute of Biology, Southern University of
Denmark, Odense Denmark
2 Department of Biology, College of Natural Sciences, Carleton University,
Ottawa, Ontario, Canada
3 Department of Applied and Engineering Physics, Cornell University, Ithaca, New
York, USA
4 Karlsbader Strasse 9, D-91083 Baiersdorf, Germany
* Author for correspondence (e-mail: ams{at}biology.sdu.dk)
Accepted 29 April 2003
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Summary |
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The ear is tuned to ultrasonic frequencies between 30 and 65 kHz, with a best threshold of around 52 dB SPL at 40 kHz, and no apparent difference between genders. Thus, drepanid hearing resembles that of other moths, indicating that the main function is bat detection. Two sensory cells are excited by sound stimuli. Those two cells differ in threshold by approximately 19 dB. The morphology of the ear suggests that the two larger scolopidia function as auditory sensilla; the two smaller scolopidia, located near the tympanal frame, were not excited by sound. We present a biophysical model to explain the possible functional organization of this unique tympanal ear.
Key words: Drepana arcuata, Watsonalla uncinula, moth, Drepanidae, Lepidoptera, hearing physiology, chordotonal organ, neuroanatomy
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Introduction |
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Tympanal ears have evolved more times in the Lepidoptera (moths and
butterflies) than in any other insect order. Ears are located on the thorax
(Noctuoidea), abdomen (Pyraloidea, Geometroidea, Drepanoidea, Tineoidea),
mouthparts (Sphingoidea) and wings (Hedyloidea, Nymphalidae, Thyridoidea) (for
reviews, see Hasenfuss, 2000;
Scoble, 1995
;
Yack et al., 2000
. Ears of the
nocturnal moths Noctuoidea, Pyraloidea, Sphingoidea and Geometroidea have been
investigated physiologically, and shown to be sensitive to ultrasound
(Göpfert and Wasserthal,
1999
; Roeder,
1974
,
1975
;
Skals and Surlykke, 2000
;
Surlykke and Filskov, 1997
).
Moth ears have evolved primarily to detect the ultrasonic echolocation cries
of insectivorous bats, but in some cases have become secondarily adapted for
conspecific communication (Conner,
1999
; Fullard,
1998
). Despite their independent origins, the body ears of all
moths, except for the Drepanoidea, are structurally similar: they have a very
thin (approximately 1 µm) iridescent tympanal membrane covering an
air-filled chamber, and a simple chordotonal organ (with one to four
scolopidia) that attaches directly, in a perpendicular or slightly oblique
orientation, to the membrane's inner surface. The tympanal membrane's outer
surface is located within a protective chamber, which in turn is exposed to
the moth's exterior.
The ears of hooktip moths are structurally unique compared to those of
other Lepidoptera, and even those of other insects, by having, presumably, an
internal tympanal membrane, and scolopidia embedded within this membrane. The
superfamily Drepanoidea comprises two families: the Epicopeiidae
(approximately 25 described species) that lack ears, and the Drepanidae (the
`hook tip moths') (approximately 650 described species), with ears. The
Drepanidae are widely distributed throughout the world except for the New
World tropics, and range in size from small to large. There are three
subfamilies, the Thyatirinae (=Cymatophorinae), Drepaninae and Cyclidiinae,
and one unassigned genus, Hypsidia
(Minet and Scoble, 1999).
General descriptions of the gross morphology and/or the scolopidia innervating
the proposed hearing organ have been provided by Gohrbandt
(1937
), Kennel and Eggers
(1933
), Minet
(1985
) and Scoble and Edwards
(1988
). The proposed tympanal
membrane of the drepanid ear is not exposed to the moth's exterior, but rather
is located internally, appearing as a partition wall between two air-filled
chambers. This characteristic structure is consistent throughout the drepanid
family (Minet and Scoble,
1999
). Early postmortal Methylene Blue studies described four
`inverted' scolopidia (however, see our results with vital staining) between
the tympanal membrane layers (Kennel and
Eggers, 1933
). Preliminary behavioural observations suggest that
drepanids react to high-pitched sounds
(Gohrbandt, 1937
;
Treat, 1962
) indicating that
they have ears that function as bat detectors. However, a sense of hearing in
drepanids has not yet been validated experimentally. In the present study we
test the hypothesis that hooktip moths possess ultrasound-sensitive hearing
organs, using neuroanatomical and neurophysiological techniques.
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Materials and methods |
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Morphology
The peripheral nerve branches and tympanal nerve were identified using
Janus Green B (Yack, 1993).
The thoracic and abdominal connectives were exposed using a dorsal approach
(cf. Roeder, 1966
), which
involved removing the mesothoracic scutum and scutellum along with the
attached flight musculature. Following this dissection, the body was cut in
half in a sagittal plane (leaving the ganglia intact on one side) and pinned
to Sylgard (Dow Corning Corporation, Midland, MI, USA) in a Petri dish. A few
drops of 0.02% Janus Green B were applied to the peripheral nerve branches of
the fresh preparation, and replaced after 1-3 min with fresh saline
(Paul, 1974
). The stained
nerve branches were drawn with a Wild M5 (Leica Microsystems Inc.,
Bannockburn, IL, USA) dissection microscope and drawing tube attachment. This
procedure was repeated until the nerve branches of interest were traced to
their peripheral targets. Tympanal membranes were imaged with a compound
microscope (Leitz Aristoplan with fiber optic illumination; Leica Microsystems
Inc.) and a digital image acquisition system [KAPPA Image Base software and
DX30 CCD camera (C)]. Tympanal chambers were sputter-coated with
goldpalladium and examined with a JSM-6400 scanning electron microscope
(JEOL, Peabody, MA, USA). Anatomical nomenclature used for muscles, nerve
branches and tympanal structures follows earlier conventions
(Gohrbandt, 1937
; Hasenfuss,
1997
,
2000
;
Nüesch, 1957
).
Staining of tympanal sensilla was executed by injecting a Leuco-methylene
Blue solution into the living animal. A freshly prepared Methylene Blue
solution in water (3% w/v) was boiled briefly to destroy colloidal complexes
and then reduced with sodium formaldehyde sulfoxylate (Rongalit BASF; Mount
Olive, NJ, USA). The slightly yellowish stain solution was diluted with an
aqueous solution of glucose (10% w/v) to which a 0.2% thionine (w/v) was
added, and then injected. After 5-15 min incubation, the specimens were
prepared by pinning the parts in position on cork plates and then fixed with a
solution of ammonium molybdate in water (10% w/v) overnight. Further details
are described in Hasenfuss
(1973).
A complete series of cross sections 72 µm thick were made from the abdominal base of a female D. arcuata fixed in Carnoy, embedded in celloidine, stained with Mallory's Phosphotungstic AcidHematoxylin, and mounted in Canada Balsam.
Electrophysiology and sound stimuli
The physiological response of the sensory cells was studied using
conventional extracellular techniques. Recordings were done in Odense, Denmark
and at Cornell University, New York. The moths were dissected using a dorsal
approach that exposes the nerve 1N1, which contains the tympanic axons
(Fig. 2A). The nerve was hooked
onto an extracellular tungsten electrode. A silver reference wire was placed
in the abdomen.
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In Denmark the action potentials were filtered (0.1-5 kHz band pass and 50 Hz notch filter), amplified (custom-built amplifier) and broadcast through an audio monitor, displayed on an oscilloscope and recorded onto a Sony TCD-D8 Dat tape recorder (Sony Corporation, New York, NY, USA; 48 kHz sampling rate). A Zephiro board (Zephiro Acoustics, USA; company no longer exists) was used to transfer the digital data from the Sony Dat to a computer for analysis. The stimuli were ultrasonic sound pulses, produced by multiplying a trapezoidal gating pulse with the continuous sinusoidal output from a Hewlett Packard 3314A digital function generator (HP, Palo Alto, CA, USA). The resulting pulses were of 10 ms duration and 0.5 ms rise/fall time and were repeated at 1 Hz. The pulses were amplified (Xelex Power amplifier, Stockholm, Sweden) and broadcast from a Technics Tweeter (EAS10TH400B; Secaucus, NJ, USA) 40 cm from the preparation. The system was calibrated using G.R.A.S. 1/4'' microphones (Type 40BF without grid) and a G.R.A.S 12AA amplifier (Vedbaek, Denmark).
At Cornell University the signal from the hook electrode was amplified and band-pass filtered (0.3-5 kHz, 40 dB/decade falloff) using an A & M Systems Model 1800 amplifier (Carlsborg, WA, USA). The amplified signal was sent to a PC for digitization (10-50 kHz). Stimulus waveform generation, data acquisition and data analysis were done using Matlab software (Mathworks, Inc., Natick, MA, USA) in conjunction with a multi-function I/O board (National Instruments PCI-MIO 16E; Austin, TX, USA). Stimulus waveforms were attenuated using a programmable attenuator (Tucker-Davis System II PA4 module; Alachua, FL, USA), and then amplified (Harmon Kardon HK6100; Woodbury, NY, USA), before being sent to a speaker (Technics EAS10TH400B) 30 cm from the animal. Pulses were 5 or 30 ms in duration, with 100 µs rise/fall times. The system was calibrated from 5-100 kHz using a Bruel & Kjaer Type 4135 (Norcross, GA, USA) 1/4'' microphone and accompanying amplifier.
Stimulus intensities were measured at the moth's position in both set-ups, and given in dB SPL relative to 20 µPa (rms).
The threshold was defined as the sound pressure level (dB SPL) sufficient to elicit 1-2 spikes within the first 5-10 ms after stimulus onset in at least 9 of 10 stimulations. For audiograms, thresholds were determined in 5 kHz steps from 10 to 60 kHz and 10 kHz steps from 70 to 100 kHz. Thefrequencies were presented in random order and the whole sequence was always followed by two controls at the first two presentation frequencies. If they were more than 2 dB from the original values, the data for that moth were discarded.
The dynamic range of the ear was determined by stimulating at one frequency with intensities ranging from ca. 10 dB below threshold to maximum output of the speaker, usually corresponding to around +50 dB above threshold. The response was recorded to 10 stimuli at each intensity. The minimum step of the dB-attenuator was 1 dB. Rasters of spike firing times were calculated from recorded post-stimulus responses. Spikes were detected using an appropriate threshold. Repeated presentations at each amplitude were superposed. Color rasters were prepared to depict post-stimulus response versus time and stimulus amplitude, with color representing the response amplitude.
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Results |
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The tympanal nerve arises from 1N1 (nerve 1Na of
Hasenfuss, 1997), the anterior
branch of the first abdominal ganglion
(Fig. 2A), which in the
Lepidoptera has been incorporated into the pterothoracic ganglion
(Nüesch, 1957
). In D.
arcuata, 1N1 is the first nerve branch arising from the
thoracicabdominal connective, 0.62±0.19 mm (N=7) from
the posterior end of the pterothoracic ganglion
(Fig. 2A). The first branch of
1N1 innervates two ventral muscles, and the second innervates the tympanal
cavity and the lateral region of the first abdominal segment. The main branch
of 1N1 (containing both afferent and efferent units) continues to the
periphery, where it innervates the dorsal and lateral parts of the
segment.
The tympanal nerve enters the tympanal cavity medially, and runs along the
ventral margin of the tympanal frame, where it terminates in four bipolar
sense cells (Figs 2B,C,
3). Each sensory neuron belongs
to a scolopidial unit, which includes a bipolar sense cell with one or more
perineurium cells at its proximal region, a scolopale cell surrounding the
sensory dendrite, and a distal attachment cell (Figs
2B,
3). The scolopidia (numbered
1-4 from medial to lateral, after
Gohrbandt, 1937) are separated
from one another between the two compressed epithelial layers of the tympanum
(Figs 1D,
2B,C,
3). Scolopidia 3 and 4 are the
largest and span the midregion of the curved tympanum, while the smaller
scolopidia 1 and 2 occur at the median end of the sclerotized tympanal frame.
As a measure of how much the tympanum curves we measured the distance,
D, directly across the frame, and the distance along the curved
membrane, arcMem, to get the radius, R, of the circle that fits the
curved membrane at the level of the sensory cells
(Fig. 2C,D). At the level of
scolopidium 4, D was 0.197±0.031 mm and R was
0.125±0.019 mm on average (N=4). At the level of scolopidium
1, D was 0.114±0.021 mm and R was
0.077±0.019mm (N=4). At scolopidium 3, D was
0.148±0.016 mm (N=5). R was not estimated.
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The scolopidia are compressed to a thickness of 2-4 µm between the two
tympanal layers. This enabled detection of many structural details without
sectioning (Figs 2B,
3). The scolopidia exhibit all
the characteristics of both mononematic and monodynal chordotonal organs
(Field and Matheson, 1998),
having one sensory neuron per scolopidium, and the distal tip of the dendrite
inserting into a scolopale cap (Figs
2B,
3). The attachment cells join
together distally, pass the tympanal frame, continue within the concave wall
of the dorsal chamber, and attach to the integument at a point near the
posterior end of the pleural chamber. These cells are densely packed with
longitudinally oriented fibrils (probably microtubules) (Figs
2B,C,
3B). Specific attachments to
the tympanal frame were not identified. We did not observe differences between
the sexes in either the peripheral nerve topography or the innervation of the
tympanum.
In W. uncinula we observed nerve branching patterns and tympanal
receptors similar to those observed in D. arcuata. However, in
addition to the four bipolar cells, a multipolar unit was observed at the
medial and posterior edge of the tympanal frame. Whether this unit is
innervated by the tympanal branch, or a branch of the posterior nerve of the
first abdominal ganglion (nerve 1Np of
Hasenfuss, 1997), is unclear.
We did not detect a similar cell in D. arcuata.
Audiograms
Full audiograms were determined for 12 D. arcuata (8 females and 4
males). All moths were tested between 5 and 100 kHz. The ears were broadly
tuned to a frequency range from 30 to 65 kHz
(Fig. 4). The mean audiogram
showed a best frequency at 40 kHz with a threshold at 52±3.6 dB SPL
(N=12). There were no differences between males and females. The
audiograms were determined by finding the threshold for the most sensitive
auditory cell. We follow the convention of other studies on lepidopteran
hearing physiology (e.g. Roeder,
1966,
1974
;
Surlykke and Filskov, 1997
)
and name the sensory cells A-cells, A1-4 in order of decreasing
sensitivity. Thus, the audiogram depicts the threshold of A1
(Fig. 4).
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Usually spike amplitude was the same for A1 and A2 and recruitment of A2 was indicated by spikes with double height or double peaks (Fig. 5). The preparations were delicate, but in the best the threshold difference between A1 and A2 was determined at 2-3 frequencies above and below the best frequency. None of these indicated that the threshold difference changed with frequency. In a single preparation the recorded A2 spike amplitude was approximately four times that of A1 (see Fig. 6B), allowing for determination of the whole A2 threshold curve (Fig. 4, inset). These results indicate that the threshold curve of A2 is broadly tuned with lowest thresholds in the frequency range 30-60 kHz.
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Response characteristics of sensory cells and dynamic range
The threshold of the most sensitive cell, A1, was rather
stereotypic from moth to moth. The standard deviation of the threshold at 40
kHz was only 3.7 dB, and the full range of thresholds of all preparations at
this frequency, recorded in two different set-ups, was 48-57 dB SPL. However,
thresholds of A2 were more variable, ranging from +12 to +30 dB,
mean +19±5 dB (N=14), relative to the threshold of
A1. Activity of other cells, the putative A3 and
A4, was difficult to detect. In most preparations there was no
further increase in spike amplitude or spikes of double height with extra
peaks, which would have indicated recruitment of a third cell. In a few
preparations, renewed jitter in the rasters at high intensities (90-100 dB
SPL) suggested that a third cell was recruited. However, at present we cannot
unequivocally say that we had excited A3 or A4.
A2 starts saturating around 15 dB above its threshold. Hence, the
total dynamic range of the ear is around 30-40 dB (Figs
5,
6).
The dynamic response characteristics of the sensory cells were studied by increasing the intensity from 10 dB below threshold to maximum output of the speaker (around +50 dB re threshold) at a constant frequency, which was not the same for all preparations but always within the range of best frequencies (30-65 kHz). In six preparations we examined spike traces (Fig. 5) in 2 or 3 dB steps and in nine other preparations we examined color rasters (Fig. 6) in 1 dB steps. In all cases, the response increased in both amplitude and duration, reflecting the recruitment of more cells and the lengthening of response spike trains of individual cells (e.g. Figs 5, 6). Some characteristics, like A1 threshold (see above) and response latency, were rather constant throughout the preparations. In all preparations, the latency around threshold was 8-9 ms, decreasing gradually to a minimum of around 2.5 ms at +20 dB re. threshold (e.g. Figs 5, 6). In contrast, substantial variation was seen in A2 threshold (see above) and in response duration of both A1 and A2. The mean response duration determined at 50 dB above threshold from rasters of preparations stimulated with 5 ms pulses was 16 ms (N=8) with a considerable S.D. of 5 ms. Of the eight preparations, four showed response durations lasting no more than approximately 11-13 ms through the entire intensity range tested (e.g. Figs 5, 6A). In one it was 16 ms, and in three the response duration increased greatly to 21-22 ms at intensities above approximately +30 dB relative to the threshold of A1 (e.g. Fig. 6B). In one preparation there was a large enough difference between A2 and A1 spike amplitudes to permit identification of individual spikes, and in this case it was clear that both A1 and A2 spikes contributed to the long response duration at high intensities (Fig. 6B).
In a few of the preparations we noted spikes from a cell that was
apparently not affected by sound, resembling the activity of a tonically
active cell (the so-called B-cell), that is prominent in recordings from
noctuoid, geometroid (Roeder,
1974) and pyraloid (Skals and
Surlykke, 2000
) tympanic nerves. Where this cell was most
conspicuous the spike amplitude was comparable to the amplitude of the
A-cells. In other preparations we recorded no activity from such a cell.
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Discussion |
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Morphology
The general morphology of the external ear structures in both D.
arcuata and W. uncinula resembles that reported for other
Drepanidae (Gohrbandt, 1937;
Kennel and Eggers, 1933
;
Minet and Scoble, 1999
). We
noted no variation between the sexes in either D. arcuata or W.
uncinula. This is in accordance with observations made by Gohrbandt
(1937
) for several other
drepanid species.
Our results show that the tympanal ears of both D. arcuata and
W. uncinula are innervated by the first abdominal nerve branch 1N1,
and the chordotonal organ Sc1 (Hasenfuss,
1997). Interestingly, the nervous supply to the ear in drepanids
is homologous to that of the abdominal ears of pyraloids and geometroids,
despite the fact that all three ears are completely different anatomically,
and are believed to have evolved independently
(Hasenfuss, 2000
). Thus, the
chordotonal organ Sc1 has been `recruited' as an auditory organ several times,
supporting the hypothesis that some chordotonal organs are better
`ear-candidates' than others. There may be several reasons why some
chordotonal organs in insects are better pre-adapted to become hearing organs
than others (see Yack and Roots,
1992
; Yager,
1999a
). In the Lepidoptera, the first abdominal segment is
especially densely packed with tracheal sacs, which are, in combination with a
chordotonal organ, a precondition for the evolution of tympanate hearing
organs (Hasenfuss, 2000
). There
are two chordotonal organs in the first abdominal segment, but it is always
the lateral organ that became auditory, probably because only this one is
surrounded by structures favouring transformation to a hearing organ
(Hasenfuss, 1997
).
Contrary to previous opinion (Gohrbandt,
1937), the tympanal nerve in drepanids departs from the proximal
rather than the distal region of the scolopidia, thus refuting the previously
held idea that the scolopidia were of the `inverted' type found in
Geometroidea and Pyraloidea. The attachment cells are densely packed with
longitudinally oriented fibrils (probably microtubules) (Figs
2B,C,
3B), and probably these
attachment cells were mistaken in the earlier study for the departing
nerve.
Sensory physiology
The audiograms show that drepanids are broadly tuned to frequencies between
30 and 65 kHz, with best thresholds around 52 dB SPL. At first, D.
arcuata may appear to be less sensitive than most Noctuoidea, which have
best thresholds of 30-40 dB SPL (e.g.
Fullard, 1998). However,
thresholds seem to be related to size, with larger moths having lower
thresholds (Surlykke et al.,
1999
), and most noctuoids studied have been larger than the
species of Drepanidae studied here. When comparing with extracellular
recordings from the tympanal nerves of other `bat detecting' ears, including
those of smaller noctuoids (Surlykke et
al., 1999
), pyraloids (Skals
and Surlykke, 2000
), geometroids
(Surlykke and Filskov, 1997
),
sphingoids (Göpfert and Wasserthal,
1999
) and other insects, e.g. some beetles
(Yager and Spangler, 1995
) and
most mantids (Yager, 1999b
),
the overall sensitivity of D. arcuata is similar. Whether the
sensitivity of D. arcuata reflects that of other Drepanoidea remains
to be determined.
There were no apparent differences between audiograms of males and females, reflecting the similar ear morphology of the genders. Hence, our results indicate that ears in drepanids have evolved for the same purpose as in other moths: bat detection.
Based on the ear anatomy, it would appear that sound waves reach the
internal tympanal membrane by way of two external membranes
(Fig. 1B,C). To test this we
performed a preliminary experiment, by covering the two external membranes
with vaseline. It was difficult to get both membranes covered entirely and the
effect of the vaseline varied. The specimen was inspected after each
experiment however, and in the insect where complete coverage was achieved the
auditory threshold increased by more than 40 dB. These preliminary occlusion
results corroborate earlier proposals (e.g.
Hasenfuss, 2000) that sound
waves reach the internal (= tympanal) membrane by way of the two external
membranes. However, we cannot exclude that covering and thus loading membranes
might also have an effect even if sound enters through other putative
entrances (e.g. spiracles). Further studies of the vibrations of external
membranes, and of the tympanal response with and without removal or covering
of the external membranes, are needed to understand the biophysics of this
system.
In physiological recordings of other moth ears, a spontaneously firing
multipolar cell (the B cell) is evident. In the Noctuoidea this cell is
associated with the ear, but its function is unclear, since it does not appear
to respond to sound (see Treat and Roeder,
1959; Yack, 1992
).
Although we also observed a similar unit in recordings of the 1N1 nerve of
D. arcuata, we do not believe that this activity arose from the
tympanal nerve, since we did not observe a multi-terminal cell in our
anatomical studies. It is more likely that this activity arises from a
multi-terminal cell located in a distal branch of 1N1, which supplies the
lateral body wall. Although a multiterminal unit was found in W.
uncinula, it did not appear to be supplied by the 1N1 branch, but rather
the posterior branch (= 1N2).
Relating physiology to morphology, and the role of the curved
tympanal membrane
The anatomical results show that there are two larger scolopidia embedded
in the tympanum and two smaller scolopidia more closely associated with the
margin of the sclerotized tympanal frame. In the morphology section we
numbered the scolopidia 1-4 from medial to lateral, after Gohrbandt
(1937), i.e. 1-2 for the two
small cells and 3-4 for the two large cells. In the physiology section we
followed the nomenclature of previous studies (e.g. Roeder,
1966
,
1974
;
Surlykke and Filskov, 1997
)
and numbered the cells A1-4, in order of decreasing sensitivity.
The position of the large cells (3 and 4 in morphology) within the tympanic
area suggests that they should sense tympanal vibrations much more effectively
than the two small cells (1 and 2), indicating that A1 and
A2 (following Roeder), the two most sensitive cells, correspond to
the two large cells: 3 and 4 in morphology.
In the tympanal ears of other Lepidoptera, the scolopidia are clustered
together into a single chordotonal organ that attaches directly to the inner
surface of a taut, flat tympanic membrane. Displacements of the membrane are
believed to be directly translated into elongation and shortening of the
scolopidia (Hasenfuss, 2000),
particularly in the region of the scolopale cell and dendritic cilium, where
sensory transduction is thought to occur
(Field and Matheson, 1998
). In
drepanids, the relationship between the scolopidia and the tympanal membrane
is completely different, since the scolopidia are embedded between the two
closely compressed layers of the tympanal membrane. If the membrane were flat,
vibrations would only result in minor length changes of the embedded
scolopidia. Therefore, we suggest that the curvature of the tympanic membrane
in Drepanidae is a biomechanical adaptation to sensory transduction, required
by the encapsulation of the scolopidia within the membrane. We use Laplace's
law modified for a cylindrical membrane (for details, see
Hasenfuss, 1999
) to predict how
pressure changes affect the curvature of the membrane, and thus the length of
the embedded scolopidia (Fig.
7). The curvature of the membrane is correlated to the inverse of
the radius, R, of the circle that follows the curvature of the
membrane. If the membrane is flat, R=
and 1/R=0. If
the membrane is a half circle then the distance across the frame, D,
is the diameter of that circle, and R is equal to D/2
(Fig. 2D). For a given change
in pressure, length changes of the scolopidia will increase with increasing
curvature of the membrane. The curvature of the drepanid tympanic membrane
(mean D/2R=0.79 and 0.74 at the levels of scolopidium 4 and
1, respectively) would cause small pressure changes to be translated to
substantial length changes of the scolopidia, according to the model
(Fig. 7). From the model it
also follows that for small pressure variations
pD/2
=
arcMem/D
arcMem=
pD2/2
.
Thus, changes in arcMem are proportional to D2, and
therefore length changes are not only proportional to the curvature, but also
to the actual diameter of the membrane at the level of the scolopidia. Using
our results for D and curvature, the model predicts that
approximately twofold more pressure change should be required to give the same
length change at the level of scolopidium 3 compared to scolopidium 4.
However, the measured threshold difference between A1 and
A2, was around 19 dB, corresponding approximately to a tenfold
pressure difference. Thus, while the model offers a working hypothesis that
relates sensory physiology to two of the distinct morphological
characteristics of the drepanid ear, the encapsulation of the sensory cells
and the curvature of the tympanum, there are obviously other factors involved
in addition to dimensions and curvature. These may include differences in
tension across the membrane, or resonance and other effects of the air volume
above and below the membrane. Confirmation of the physiological
characteristics of individual units in the ear must await further studies
involving intracellular recording and staining techniques.
|
Evolution of moth ears
Moth ears exemplify that even the simplest of insect ears provide
sufficient adaptational value as bat detectors. They have one (Notodontidae,
some Sphingidae) two [Noctuoidea (other than Notodontidae), Uraniidae], or
four (Geometroidea, Pyraloidea, Drepanidae) scolopidia (for reviews, see
Miller and Surlykke, 2001;
Scoble, 1995
;
Yager, 1999a
). In those with
two or more sensory cells, one cell (A1) is always the most
sensitive, and the others are decreasingly sensitive in steps of approximately
10-20 dB. Since all moth ears studied to date are incapable of frequency
discrimination, the function of having multiple cells is unknown. Although it
has been speculated that in the Noctuoidea, A2 triggers the switch
from a negative phonotaxis behaviour to an evasive flight maneuver, there is
no direct evidence for this, and it is possible that A1 alone is
responsible for triggering bat avoidance behaviours (e.g.
Miller and Surlykke, 2001
).
This argument is supported by the fact that notodontids, with only one
auditory cell, appear to exhibit the same bimodal evasive behaviours as moths
with 2-4 cells (Surlykke,
1984
).
Since in drepanid ears only two of the four sensory cells appear to respond
to sound at all, this may support the hypothesis that, in ears that function
primarily as `bat detectors', there may be a cost, either functionally or
metabolically, to having extra sensory cells. Comparative anatomical and
developmental studies indicate that in ears that function as `bat detectors',
there is a trend from having a higher number of cells in the primitively
atympanate state, to a lower number of cells in the tympanate state. In
contrast, insect ears that function primarily to identify and localize calling
songs of other insects are generally more complicated, with an increasing
number of cells from the atympanate to tympanate condition (for discussion,
see Yack et al., 1999).
In the Drepanidae we recorded acoustic activity from two cells
(A1 and A2), and, based on morphology, we assume that
these represent scolopidia 3 and 4. What then might be the significance, if
any, of scolopidia 1 and 2? We propose that they may have retained their
functional role as proprioceptors. In drepanids the four scolopidia are
separated spatially within the tympanum, which may have allowed scolopidia 1
and 2, close to the frame, to maintain their original function. In accordance
with this hypothesis are the facts that: (i) morphologically 1 and 2 do not
appear degenerate, and (ii) the very long and conspicuous attachment cells
extend far outside the tympanum and are attached to the integument at a point
postero-ventrally to the spiracle, not far away from the attachment site of
the homologous organs atympanate moths
(Hasenfuss, 1997). The presumed
sensitive neuronal zone (i.e. the dendritic cilium) of scolopidia 1 and 2 are
so near the margin of the frame that it seems possible that these neurones are
stimulated by pulling movements of the attachment cell fibrils, rather than by
movements of the tympanum. In contrast, the sensitive zone of scolopidia 3 and
4 are within the tympanal area and are thus possibly not affected by pulls of
these fibrils, but rather by vibrations of the tympanum. Physiological
recordings from individual units are required to answer these questions.
The Drepanidae provide yet another unique solution to the way insects have come up with an ear. Our study supports the hypothesis that drepanid ears, like those of other nocturnal Lepidoptera, function primarily to detect bats, since the ears are sensitive to ultrasound, and are equally well developed in both sexes. Further, our results suggest that the most important physiological characteristic of all moth ears is the threshold of the most sensitive sensory cell, A1, which is remarkably similar physiologically in all ears, despite their unique morphologies and independent origins. This appears to be where the selection pressure exerts its effect, while other characteristics such as external morphology, details of physiology, and threshold of less sensitive sensory cells, are subject to less selection pressure. The fact that Drepanidae have functional ears with internal tympanal membranes also opens the door to finding ears in other insects that are not so obvious from their external anatomy.
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