Download Hearing in Geometrid Moths

nearly completely by the varying local O3 production. These results lead
us to the conclusion that, at least during the period investigated, stratospheric or higher tropospheric contributions could hardly play an important role with regard to the high summer ozone levels found in the context
of an urban area.
Naturwissenschaften 84, 356–359 (1997)
We thank the Vienna Municipal Department (MA 22-Environmental Protection) for providing the Ozone data.
1. Brost, R.A., Feichter J., Heimann M.:
J. Geophys. Res. 96, 22, 423–22 445
(1991)
2. Feely, H.W., Larsen, R.J., Sanderson,
C.G.: J. Environ. Radioactivity 9, 223–
249 (1989)
3. Larsen, R. J.: J. Environ. Radioactivity
18, 85–87 (1993)
© Springer-Verlag 1997
Hearing in Geometrid Moths
Annemarie Surlykke, Mads Filskov
Center for Sound Communication, Institute of Biology, Odense University,
DK-5230 Odense M. Danmark
Received: 9 December 1996 / Accepted in revised form: 2 June 1997
Ears sensitive to ultrasound have
evolved several times among the families of nocturnal Lepidoptera, including at least once in the Geometridae
[1, 2]. The ears of moths appear to
have evolved with one main purpose,
namely the detection of the calls of
echolocating bats [3]. Only a few species use their hearing for sexual communication, presumably as a secondary adaptation [4]. Hearing organs occur throughout the family of Geometridae (c. 20 000 species) except in a
few wingless females where they are
lost secondarily. The tympana at the
base of the abdomen are best seen
when the abdomen is removed and
viewed end-on. On the inside the two
Correspondence to: A. Surlykke
356
hearing organs are served by a common tracheal air sac. A sclerotized
bridge, the ansa, which is unique for
Geometridae, stretches across the tympanic membrane [1, 5, 6]. The scoloparium is suspended between the ansa
and the tympanic membrane and contains four sensory cells, A1–4. Their
dendrites attach to the tympanum and
fold back on themselves. Since the
scolopales are therefore directed away
from the tympanum, the scoloparium
is said to be inverse [5, 6]. The
unique morphology of the ear supports the contention based on phylogeny that the ears in geometrids
evolved independently [1, 5]. Hence
geometrid ears are neither homologous to the abdominal ears of Pyralidae nor to the much more thoroughly
studied thoracal ears of Noctuoidea
with their two sensory cells. Only lit-
4. Lal, D., Peters, B., Handb. Phys. 46, 551–
612 (1967)
5. Hötzl, H., Rosner, G., Winkler R.: Naturwissenschaften 78, 215–217 (1991)
6. Dutkiewicz, V.A., Husain, L.: Geophys.
Res. Lett. 6, 171–174 (1979)
7. Österreichische Akademie der Wissenschaften, Kommission für Reinhaltung
der Luft: Photooxidantien in der
Atmosphäre-Luftqualitätskriterien Ozon,
p.10.11. Vienna:1989
tle is known about hearing in different
geometrid species [7, 8]. However, it
seems likely that it is the predation
pressure from bats which has
prompted the evolution of ears independently both in the Noctuoidea and
in the Geometridae. There are no published reports of sound production in
geometrids. In addition, batlike ultrasound pulses elicit clear evasive maneuvers in geometrids ([9], own observations). The geometrids have relatively large wings and fly more
slowly; thus they are presumably subject to at least as strong a selection
pressure from bats as are noctuoids.
Therefore we attempted to determine
the auditory characteristics of some
geometrid moths and to compare their
hearing capability with noctuid moths.
Thus we hope not only to increase the
knowledge of geometrid audition but
also to provide further insight into the
general principles of evolutionary interaction between moths and bats.
There are six subfamilies of Geometridae with around 300 species in
Denmark. We determined the audiograms of seven species of two subfamilies, Geometrinae and Ennominae.
All the moths we chose for this study
are relatively large, with wing spans
between c. 35 and 47 mm [10]. Thus
they are among the acoustically most
conspicuous geometrids and therefore
presumably subject to maximum predation pressure by bats. We caught
the moths in light traps in the vicinity
Naturwissenschaften 84 (1997)
© Springer-Verlag 1997
Table 1. Threshold of A1 in dB SPL at the best frequency, and the thresholds of the three less
sensitive acoustic sensory cells in dB relative to the threshold of A1. (n number of raster plots
used to determine the thesholds of A2–4)
Fig. 1. Audiograms for: upper panel, the
three Ennomos species, E. alniaria (n = 12),
E. autumnaria (n = 12), E. fusantaria
(n = 1); middle panel, B. betularia (n = 29)
and O. luteolata (n = 1); lower panel, G. papilionaria (n = 4) and C. elinguaria (n = 4).
Whenever n > 1 the species mean is given.
Vertical bars, typical standard deviations
Naturwissenschaften 84 (1997)
Species
A1 dB SPL
B.betularia (n = 9)
E.alniaria (n = 1)
E.autumnaria (n = 7)
C.elinguaria (n = 3)
37±8
42±4
37±4
35±5
of Odense University (Denmark). We
used one Geometrinae species, Geometra papilionaria (L.), and six Ennominae species, Biston betularia
(L.),
Ennomos
alniaria
(L.),
E.autumnaria (Wernb.), E.fuscantaria
(Hw.), Crocallis elinguaria (L.), and
Opisthograptis luteolata (L.). Most
moths were dissected ventrally to reveal the tympanic nerves, which enter
the abdominal connective just caudal
to the metathoracic ganglion. For
comparison some moths were dissected from the dorsal side, thus
opening the tracheal air sac. The two
dissection methods gave the same
thresholds. Activity in the tympanic
nerve was recorded by an extracellular tungsten hook electrode. The nervous response was sampled (10 kHz
sampling rate) on a computer. The
sound stimuli were 5-ms pulses generated by a computer controlled function generator (Hewlett Packard
3314A). The pulse repetition rate was
1 Hz. Audiograms were determined
automatically using the computer to
control the sound frequency and intensity according to the response of
the sensory cells. The threshold criterion, based on an average of five stimulations, was two spikes above
background level in a 16-ms window
from 4 to 20 ms after stimulus onset.
We tested frequencies between 5 and
100 kHz in 5-kHz steps. Intensities
are given in decibels SPL relative to
20 lPa (rms).
All seven species had functional ears
with best frequencies (BF) between
20 and 30 kHz (Fig. 1). All audiograms were broadly tuned, with
thresholds increasing slowly towards
higher frequencies. The Q10dB values
ranged from 0.9 to 1.6. The thresholds at BF were between 35 and
45 dB SPL for the A1 cells. The only
species of the Geometrinae, G. papi-
© Springer-Verlag 1997
A2 dB re. A1
+15±2
+15
+12±2
+17±3
A3 dB re. A1
+26±2
+25
+22±4
+27±2
A4 dB re. A1
+37±2
+33
+31±4
+38±4
Fig. 2. Raster plot of spikes in the acoustic
sensory cells in B. betularia at intensities
from 29 to 89 dB SPL. Horizontal line, 5-ms
stimulus pulse; arrows, estimated thresholds
of the four sensory cells. A postexcitatory
suppression of A1 and A2 is seen above
around 50 dB SPL. The response of A3 and
A4 outlasts the stimulus by up to 25 ms
lionaria, was the least sensitive species. The thresholds of the Ennominae
species varied a great deal from the
most sensitive species, C. elinguaria
and O. luteolata, to the least sensitive
species, E. fuscantaria, which is only
slightly more sensitive than G. papilionaria (Fig. 1). Thus from our results we cannot say whether the Geometrinae in general are less sensitive
than Ennominae.
It was impossible to discriminate between the spikes of the four A cells
since all spikes had similar shape and
size. Therefore we determined the
thresholds of the three less sensitive
sensory cells, A2–A4, and the dynamic range of the ear from raster
plots of spike activity. Rasters depicting a large amount of data in one plot
allow for visual extraction of patterns
that cannot be seen from single recordings. We made raster plots for
357
four species, B. betularia, C. elinguaria, E.autumnaria, and E. alniaria. Only the time of occurrence of the
spikes was saved on the computer and
later displayed as dots in a raster plot.
The spikes were detected by the computer after manually adjusting the
spike detection threshold each time
we started a new recording. Spike
times were sampled 5–15 times at
each intensity. The intensity was increased in 1-dB steps from c. 5 dB
below threshold up to c. 90 dB SPL,
thus covering an intensity range of
around 50 dB. The frequency was
usually the BF. The raster plots display the spikes as almost vertical columns, indicating that the latencies and
interspike intervals are relatively constant (Fig. 2). The columns are disrupted by three horizontal bands of
more randomly occurring dots at certain intensities, which we interpret as
the threshold levels for the three less
sensitive acoustic sensory cells, A2–
A4 (arrows in Fig. 2, Table 1). These
horizontal bands of disturbance are
due to the longer and less stable latencies and interspike intervals near the
individual thresholds of the four A
cells.
In some animals we also saved the
whole sampled nerve response at different intensities as a control of our
interpretations of the raster plots. Just
above threshold the activity of only a
single sensory cell, A1, was seen. Increasing the intensity from +12 to
+17 dB relative to the threshold for
A1 elicited the activity of a second,
less sensitive cell, A2, revealed by the
appearance of spikes of double height
or with double peaks [11]. Using this
method we made whole threshold
curves of the A2 cell in two specimen
of E. alniaria and one E. autumnaria.
In each individual the A2 curve was
13–15 dB above and parallel to the
A1 curve over the whole frequency
range from 5 to 100 kHz. Thus the
A2 thresholds determined in this way
confirmed the A2 thresholds estimated
from the raster plots. In a few recordings spikes with triple height or triple
peaks could be used to estimate A3
thresholds. These thresholds also
matched the A3 thresholds determined
from the raster plots. Hence we assume that the raster plot method is valid also for A4 where recognition by
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direct inspection is impossible because of the very complicated spike
pattern.
The raster plots revealed some of the
physiological characteristics of the
four sensory cells. The response duration of the two more sensitive cells
A1 and A2 is approximately 10 ms
(seven or eight spikes). The response
is followed by a postexcitatory suppression starting c. 15 ms after stimulus onset and lasting around 15 ms.
This suppression is seen most clearly
between 50 and 70 dB SPL in Fig. 2,
where A3 and A4 are not yet recruited. At high intensities the response duration increases, indicating
that the two less sensitive cells A3
and possibly A4 have another response pattern with a long afterdischarge outlasting the stimulus by
around 25 ms. All four species
showed this.
The minimum latency of A1 is
reached c. 5–10 dB above its threshold. A2 has the same minimum latency as A1. Thus at intensities exceeding the A2 threshold by more
than approximately 5 dB the spikes of
those two cells are synchronized
forming one column in the raster
plots. The latency is then rather constant up to around the threshold of
A3, where it starts decreasing again,
thus indicating that A3 (and A4) have
a shorter minimum latency than A1
and A2. This explains why the first
vertical columns divide into double
columns at intensities exceeding the
A3 threshold by more than around 5–
10 dB. Double columns were seen at
high intensities in the raster plots of
three of the species, B. betularia, E.
alniaria, and C. elinguaria, whereas
the raster plots of E. autumnaria
showed single columns even at the
highest intensities, indicating that in
this species all four cells have the
same minimum latency. Inspection of
spikes in samplings of whole responses in E. autumnaria confirmed
this conclusion.
The total dynamic range of the ear is
45–50 dB in all four species. The dynamic ranges of the single cells were
estimated both from raster plots and
from direct inspection of whole nerve
responses. The number of spikes and
spike rate as a function of intensity
indicated that the dynamic range of
A1 was between 10 and 15 dB. The
dynamic range of A2 was about the
same although more difficult to determine. We could not determine the dynamic ranges of A3 and A4 with any
confidence.
The recordings clearly showed the activity of a nonacoustic sensory cell in
the tympanic nerve. In most recordings the activity was rather low, but if
the moth started to move the body
during the recording the spike rate
could exceed 700 Hz. The anatomy of
this nonacoustic B-cell [7] has not
been described in geometrids, but it
may have the same function as the Bcell in noctuid moths, where it seems
to be a stretch receptor [12].
All the tested geometrid species had
broadly tuned audiograms with BF
and thresholds at BF comparable
those of noctuoid moths from the
same geographic area [11, 13]. This
result supports our hypothesis that a
common selection pressure from bat
predation has shaped the sensitivity of
moth ears. Geometrids from Africa
[8] are somewhat more sensitive
(around 30 dB SPL at BF) than the
species that we studied. This, again,
corroborates the hypothesis of a common selection pressure since tropical
noctuoid species are also more sensitive than temperate ones, probably an
adaptation to the more diverse and
numerous bat fauna in the tropics [3].
The notation A1–4 is based simply on
the thresholds and thus may not denote the same cells in different species. However we find this possibility
less likely since the raster plots revealed very similar response patterns
both regarding threshold differences,
latencies, and response durations at
different intensities in all species investigated. The thresholds of the four
cells are equally spaced in geometrids, in contrast to the Pyralidae,
where the two more sensitive of their
four cells have almost the same
thresholds (N. Skals, personal communication). We found dynamic
ranges of 10–15 dB for the individual
A-cells, which is considerably less
than the 20 dB reported earlier [7].
The total dynamic range of the fourcelled geometrid ear is only a little
larger than the 35–45 dB dynamic
range of the two-celled noctuid ear
[7]. Hence the overlaps between the
Naturwissenschaften 84 (1997)
© Springer-Verlag 1997
dynamic ranges of the four cells are
comparable to the overlap between
the two cells of the noctuid ear. Geometrids show evasive behavior differentiated on basis of intensity [9], but
whether the more complicated ear and
the differences in response patterns of
the four cells are reflected in a more
differentiated evasive behavior than
that found in noctuids remains to be
studied. In addition, it is unknown
how stimulus repetition rates affect
behavioral responses. There is a clear
lack of detailed behavioral data on
evasive maneuvers of geometrids to
bat ultrasound.
Naturwissenschaften 84, 359–362 (1997)
We thank Niels Skals, Asher E. Treat
and Lee Miller for valuable comments
on the manuskript. The study was
supported by the Danish National Research Foundation.
1. Minet, J.: Annals. Soc. ent. Fr. (N. S.)
19, 175 (1983)
2. Scoble, M.J.: The Lepidoptera. Form,
function and diversity. Oxford: Oxford
University Press 1992
3. Fullard, J.H.: Experientia 44, 423 (1988)
4. Spangler, H.G.: Ann. Rev. Entomol. 33,
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© Springer-Verlag 1997
Formation Process of Hopperlike b-Si3N4 Crystal
Formed by Postshock Vaporization
and Condensation of Amorphous Powder
K. Yamada
Department of Chemistry, National Defense Academy, Hashirimizu Yokosuka
239, Japan
A. B. Sawaoka
Materials and Structures, Materials and Structures Laboratory,
Tokyo Institute of Technology, Nagatuda Midori-ku, Yokohama 227, Japan
Received: 14 January 1997 / Accepted in revised form: 2 June 1997
Prism, whisker, and needle crystals of
Si3N4 – with two modifications, a
rhombohedral structure (a form) and a
hexagonal structure (b form) – have
Correspondence to: K. Yamada
Naturwissenschaften 84 (1997)
been produced on a substrate by a
chemical vapor deposition method
[1–3], thermal decomposition method
[4], and sublimation method [5].
These crystals were thought to grow
through a vapor?solid process. On
the other hand, some investigators
© Springer-Verlag 1997
7. Roeder, K.D.: J. Insect Physiol. 20, 55
(1974)
8. Fenton, M.B., Fullard, J.H.: J. Comp.
Physiol. A 132, 77 (1979)
9. Rydell, J., Skals, N., Surlykke, A.,
Svensson, M.: Proc. Roy. Soc. B. 264,
83 (1997)
10. Skou, P.: Nordens Målere. In: Danmarks
dyreliv, Vol. 2 (L. Lyneborg, ed.). Fauna
Bøger & Apollo Bøger 1984
11. Surlykke, A.: J. exp. Biol. 113, 323
(1984)
12. Yack, J.E.: J. Comp. Neurol. 324, 500
(1992)
13. Surlykke, A., Miller, L.A.: J. Insect Physiol. 28, 357 (1982)
have reported that amorphous Si3N4
filament is formed via a vapor?liquid?solid process by the
chemical vapor deposition method [6,
7].
In contrast, filament, dendrite, prism
of a and b forms, and sphere and dendrite with amorphous structure have
been formed in free space using a
postshock vaporization and condensation technique [8, 10]. This technique
uses very high residual temperatures
occurring in the central region of cylindrical sample for the vaporization
of powdered materials with high melting point. Since the residual energy is
the difference in entropies of shock
compression by shock waves and
pressure release by rarefaction waves
[9], the lower the sample density before shock compression (referred to
below as “sample density before
shock compression” to “initial density”) of the powdered material, the
larger is the residual energy, and the
higher is the residual temperatures.
Therefore in this technique the environmental conditions such as temperature, degree of supersaturation, and
359