<oological Journal ofthe Linnean SocieQ (1993), 107: 155-167. With 7 figures
Acoustic behaviour and phonotaxis in the
duetting ephippigerines, Steropleurus no brei*
and Steropleurus stali (Tettigoniidae)
J. C. HARTLEY
Department of Lije Science, Universiq of Nottingham, Nottingham NG7 2RD
Received February 1992, accepted f o r publication June I992
Both sexes of the ephippigerines Sleropleurus stali and S. nobrei can stridulate and produce
multisyllabic calls which are described. Female stridulation is in response to the conspecific male
call. In both species either sex can perform phonotaxis on the call of the conspecific member of the
opposite sex, but ignore the calls of other species. The parameters of the calls are examined with the
conclusion that the only reliably distinctive feature is the modal or carrier frequency generated
during stridulation. There are frequency differences between male and female calls in both species.
Males only perform phonotaxis on female replies generated in response to their own call, implying
that there is also some time window involved. Male phonotaxis was faster and more accurate than
that of the female. Acoustic rivalry and aggression were also noted, particularly in females.
ADDITIONAL KEY WORDS:-Stridulation
-
frequency discrimination
-
acoustic rivalry.
CONTENTS
Introduction . . .
Materials and methods
Results . . . .
Disrussion
. . .
Acknowledgement.
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. . .
References
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155
156
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163
166
166
INTRODUCTION
The normal pattern of phonotaxis in the Tettigoniidae is for a male to call and
a receptive female to move silently towards him. Females in most of the
subfamilies are incapable of stridulation. However, in two subfamilies,
Phaneropterinae and Ephippigerinae, females have stridulatory apparatus
which in each is morphologically distinct from that of the male. Many
phaneropterine females are known to stridulate in response to a male call and
the males perform phonotaxis on the female reply (Robinson, Rheinlaender &
Hartley, 1986; Heller & von Helverson, 1986; Robinson, 1990), although the
stridulatory apparatus of the female is only poorly developed. O n the other hand
ephippigerine females possess an elaborately constructed stridulatory apparatus
with a distinct file, rather like that of the male. Little was known about its use
until a response song was discovered in two species, Steropleurus stali and
*See Nole added in proof (p. 166)
0024-4082/93/020155
+ 13 $08.00/0
155
0 1993 The Linnean Society of London
I56
J. C. HARTLEY
Platystolus obvius (Hartley, Robinson & Warne, 1974). It became evident, from
that study, that there were two patterns of stridulatory behaviour in the
Ephippigerinae, reiterative singers like Ephippiger, and the sporadic singers like
S. stali. Females of the reiterative singers do not stridulate in reply to the male
call, they just move to the calling male. With the sporadic singer, P. obuius, a
female reply causes the male to start calling frequently which enabled female
phonotaxis. At that time phonotaxis experiments were not possible with S. stali,
but since then both S. stali and S. nobrei have been kept in culture. New features
in the phonotactic behaviour of these ephippigerines are now described.
MATERIALS AND METHODS
Adult S. nobrei* were collected in the Picos d’Europa, N. Spain, in 1985 and
several generations reared subsequently in the laboratory, using methods similar
to those used for Ephippiger (Hartley & Dean, 1974). Steropleurus stali were
collected in the Sierra Guadarrama, Central Spain, in 1988 and likewise
successfully cultured.
Steropleurus stali (Bolivar) and S. nobrei (Bolivar) are very similar in appearance
and are typical small examples of the genus. The generic name Steropleurus
Bolivar is used in preference to Uromenus Bolivar, following Morales Agacino
(1945) rather than Harz (1969), since U . rugosicollis is clearly morphologically,
acoustically and behaviourally quite distinct from insects like S. stali and
Steropleurus periri (Bolivar). Morphologically the two species S. stali and S. nobrei
are practically indistinguishable, in spite of positive but inaccurate indications to
the contrary in some taxonomic works. However, the males can be clearly
distinguished by their calling songs.
Sound interaction experiments were carried out in a greenhouse laboratory
with unmated 2-3-week-old adults. No acoustic screening was used, but other
active adults of the same species were acoustically isolated. A large (3 x 1 m)
formica-topped table was used for phonotaxis experiments, the position and
movement of the insects being recorded on its surface. Additional phonotaxis
experiments were undertaken in a large terylene gauze cage, 2 m long by 60 cm
square cross-section.
Sound recording was by a Q M C SM2 high frequency microphone on to a
Racal Store 4 tape recorder at 15 ips (38.1 cm s-I) and replayed at one-quarter
or one-eighth speed. The general form of the songs are presented as ‘pseudooscillograms’ in that they were traced from the screen of a storage oscilloscope by
hand. Detailed sound traces were produced and analysed on a B&K 2032 dual
channel sound analyser by Dr R. 0.Stephen. Frequencies were then determined
by measuring the wave spacing on the oscillograms generated on the B&K 2032
either directly or from subsequent plots.
RESULTS
Songs
These results are based on data from 40-50 males and 30-40 females of each
species, of different generations, reared in different densities and exhibiting
considerable variation. Between 5 and 15 calls from each individual were
*See Note added in proof (p. 166).
ACOUSTIC BEHAVIOUR IN S7EROPLEURUS
---
I57
4
C
A
4
1
5M) ms
Figure 1. Pseudo oscillograms (traced from the screen of a storage oscilloscope) of the calls of
Steropleurus stali. A, D, Male calls followed by long female replies (B, E); C, a short female reply.
recorded. Males of both species produce multisyllabic calls composed of 6- 15
syllables of increasing amplitude. In both species the females produce
multisyllabic replies. A syllable is defined as the sound produced by a single
cyclical movement of the wings, a semisyllable from the single opening or closing
movement. Duetting is considered to occur when a female consistently replies
and the male song behaviour is modified.
Steropleurus stali-the male call
The male call of S.stali (Fig. lA, D) is substantially as described previously
(Hartley el al., 1974) with 8-15 syllables in which sound may be generated on
both opening and closing strokes of the wings (Fig. 2 ) . Relatively few file teeth
are struck in each syllable, rising from two or three in the initial syllables to
about 15 in the final syllable. In each syllable the opening stoke is slower than
the closing stroke. As can be seen in Fig. 2. the opening stroke has distinct tooth
strikes, each generating a transient or brief pulse of sound composed of only 2-3
oscillations at the resonant frequency before decaying into the background noise.
The resonant or carrier frequency at this point is in the range of 8-10 kHz. The
faster closing stroke generates a frequency in the range of 15-19 kHz, possibly
forced directly by the tooth strike rate and overriding the modal frequency seen
above. The amplitude of the sound produced increases throughout the call, but
there is little difference between opening and closing semisyllables.
Steropleurus stali-the female repb
The female reply (Fig. lB, E) is usually a multisyllabic song of 8-10 syllables,
quite similar to that of the male, produced 10-400 ms after the end of the male
call. Occasionally females produced a short reply song (Fig. 1C) of 1-3 syllables
as noted by Heller (1988). This seemed to be associated with the first females to
mature in a population. Later, when there were several active adult females, the
long reply song predominated. The short song has the appearance of being just a
shorter and more erratic version of the long song. In both long and short songs
sound is generated on both the opening and closing wing strokes, although the
movements are irregular. Figure 3 shows part of a female reply in detail. The
carrier frequency is around 14-15 kHz. In the opening semisyllable the
amplitude is low and the carrier frequency often obscured by irregularities in the
tooth strike rate. The closing stroke generally seems to produce a greater
amplitude with the carrier frequency distinct.
B
-
Figure 2. A, Oscillogram (plotted from the B&K 2032) of a single syllable from central part of the
call of a male Stcropleurus stdi of form as shown in Fig. ID; B, expanded oscillogram of part of A,
showing the last two tooth impulses of the opening stroke the begining of the closing stroke. Between
the distinct tooth impulses of the opening stroke is a certain amount ofecho; the distinction between
separate tooth pulses is obscured in the closing stroke. The frequency generated by the oscillations in
the opening stroke is 9f 1 kHz and is approximately doubled in the closing stroke. Time marker
lines- I ms, vertical axis-linear amplitude in arbitrary units.
Steropleurus nobrei-the male call
The calling song of male S. nobrei consists of a sequence of 6-8 brief pulses
followed by two longer pulses (Fig. 4A). The brief pulses are semisyllables each
comprising 6-8 tooth impacts, generating brief transients as in S. stali, produced
on the opening stroke of the wings (Fig. 5A). The first of the longer pulses is
produced by a full opening stroke of the wings followed by a slow closing stroke
in which 25-30 teeth are struck in a very ‘deliberate’ manner, producing what is
termed here the major semisyllable. High speed video recordings revealed that
the insect was using the same part of the file for each of the minor syllables, the
wings were then opened fully during the opening stroke of the major syllable so
that most of the teeth on the file could be struck on the closing stroke. Again only
brief transients are produced (Fig. 5B). The male call was sometimes followed by
a few erratic pulses, here termed the secondary song (Fig. 4B), which were
produced particularly after establishment of a duet with a responding female
and following her reply. The modal frequency generated in all parts of the call
by an individual was the same, within the range 13-16 kHz.
Steropleurus nobrei-the female repb
Steropleurus nobrei females generate two types of reply song. The type A chirp
(Fig. 4C), consisting of 2, sometimes 4 or 6, pulses generated by closing strokes of
the wings, was produced between 10 and 140 ms after the end of the main part of
ACOUSTIC BEHAVIOUR IN STEROPLEURUS
159
H
A
Figure 3. Oscillograms of parts of the female Sleropleurus slnli reply call: A, syllable from the short call
(as in Fig. IC), showing both opening and closing stroke; B, expanded ( x 2) part of a showing that
the same frequency is generated in each part but the opening semisyllable is of lower amplitude.
Scales as Fig. 2.
male chirp. Each pulse lasted less than 20 ms. This chirp was usually produced
when the female was more than 50 cm distant. The type B chirp (Fig. 4D),
usually produced when the female was close to the male, lasted about 220 ms
and consisted of 5-7 brief double pulses, presumably pairs of semisyllables
generated by opening and closing actions of the wings. The type B chirp was
emitted some 1.5-3.0 s after the male chirp. As in the male the sound consists of
a series of brief transients (Fig. 6) which are the same for either chirp type. Also
as in the male the main emphasis seems to be on the closing stroke which is
slower and of greater amplitude.
--f-+---t-t-
~
t.mww+-
.4
D
C
L
J
5W mo
Figure 4. Pseudo oscillograms of calls of Steropleurus nobrei. A, The male call showing 8 minor
semisyllables produced by repeated opening of the wings (no sound is produced on the closing
strokes), followed by another longer opening semisyllable and then the major semisyllable produced
by wing closure; B, some of the erratic pulses of the secondary song; C, the type A female reply with
4 pulses; D, the type B female reply with distinct opening and closing pulses.
J. C. HARTLEY
I60
1.0
0.5
0
-0.5
-1.0
i
4
A
4
-
B
Figure 5. Oscillograms of a minor (A) and part of the major (B) semisyllable of a male call of
Sferopleurur nobrei. Scales as Fig. 2.
200 m
1
200 m
100 m
0
-100m
I
1
B
Figure 6. Oscillograms of A, opening and B, closing semisyllables of a female reply of Sfnoplcurus
nobrci. I t is clearly evident that the closing stroke is slower but generates much louder transients.
Scales as Fig. 2.
ACOUSTIC BEHAVIOUR IN S'TEROPLEURUS
161
Steropleurus nobrei interactions
The following sequences of calling were observed:
M
M
M
M
(main) __
(main)
(main)
(main)
M (main)
~
~
~
F (A)
F (B)
F (A) __ M (secondary)
F (A) __ M (secondary)
M (secondary) -~
F (A) __ M (secondary)
F (€3)
There is considerable variation in the latter parts of the sequence.
General song characteristics
The number of syllables emitted by male S. nobrei was related to the acoustic
environment. Solitary males produced the longest calls, 8-1 1 (mean 9.1)
syllables in the main call and usually no secondary call. Males receiving female
replies (type A ) from distances greater than 60 cm emitted 7-10 (mean 8.6)
pulse chirps, and in established duets at less than 60 cm the syllable number was
reduced to 4-10 (mean 5.9). No such variation was found in S. stali although
some longer male calls elicited longer female replies.
The song characteristics of both species are set out in Table 1.
Calling rate
The chirping rate of solitary individuals of both species was low, with the
number of chirps ranging from 10 to 90 per hour during the morning at
temperatures between 2 1" and 30°C. Acoustic activity declined rapidly after
mid-day, with most insects becoming silent. It was also depressed by ambient
temperatures above 30"C, but otherwise the calling rate was not particularly
temperature dependent. The presence of other calling males increased the chirp
rate considerably. With two males, song alternation occurred at a rate
equivalent to 120-300 chirps h-' in S. stali and slightly slower at 90-190 chirps
h-' in S. nobrei. In a male-female duet the call rate increases to between 300 and
800 chirps h-I.
Phonotaxis
Unlike previously studied species, both sexes can perform phonotaxis on. the
song of the opposite sex. Phonotaxis was always initiated by the male calling. A
TABLE
I . Song characteristics
Steropleurus stali
80 male calls
55 frmalr replies
Stprripleuru~nobrri
90 male main calls
40 female type A replies
30 &male type B rrplies
30 male secondary cells
alter female ( A ) reply
Delay
(ms)
Pulses
per cell
Duration
nla
8-15
8-10
250-370
150-230
8-10
15-19
14-15
14-15
8-11
2, 4, 6
8-10
300-500
60- 180
200-220
13-16
16-19
16-19
13-16
16-19
16-19
80-200
13-16
13-16
0-400
nja
10-140
0-3000
80-200
2-4
(msi
Frequency (kHz)
opening/closing stroke
J. C. HARTLEY
I64
acoustic interaction across the species boundary and certainly no phonotaxis.
Therefore it must be assumed that the songs are sufficiently different to avoid
confusion between these two species. Since also, within a species, males will
perform phonotaxis on females or vice versa but not on members of their own sex
and that the song rate increases when a bisexual duet is established, the songs of
either sex must be sufficiently identifiable as being male or female.
Features that could make the male calls identifiable are carrier frequency,
pulse number, pulse repetition rate, and overall chirp pattern. These same
features could be used to distinguish the female reply, perhaps depending on
whether it falls within an appropriate time window, as with phaneropterines
(Robinson et al., 1986; Heller & von Helverson, 1986).
Looking at these features in turn we find that there are frequency differences
between the species and to some extent between the sexes, but since these arise
from very brief pulses they may be difficult to resolve (Hartley & Stephen,
1992). It is well established that the bush-cricket ear is able to resolve frequency
and that single transient impulses evoke highly synchronized activity in the
auditory neuropile, although the high frequency elements of a call cannot be
resolved by single receptor cells (Rossler et al., 1990). Yet the nature of the
oscillations produced by each tooth impact in comparison with many other
Tettigoniidae (Keuper et al., 1988; Rossler el al., 1990) suggests that the highly
damped brief transient has evolved as a feature in the Ephippigerinae. This is
particularly so of the major syllable of S. nobrei where each tooth strike produces
a distinct brief transient of no more than three distinct oscillations at the carrier
frequency, before the sound merges with background. Since this syllable is so
elaborately produced and represents the major energy contribution of the call, it
must be of considerable importance in communication. As indicated, frequency
resolution of such brief high-frequency transients presents a problem to any
analogue detection system. It is only by producing resonance in a tuned acoustic
filter that frequency can be determined. Thus a signal of only a few brief
transients introduces a degree of frequency uncertainty into the system.
Frequency uncertainty (df) is given by the equation df.dt = 1 where dt is the
duration of the transient. This is equivalent to df = f/n where n is the number of
cycles in the transient. (See Hartley & Stephen, 1992 for further discussion of
this problem.) The calculated degrees of uncertainty for the two species are given
in Table 3.
This shows that there is some potential for overlap between the sexes and
species in the broadcast sound. Hartley & Stephen (1992) in discussing this
problem, suggest that the ear structures can act as an acoustic filter capable of
TABLE
3. Calculated frequency uncertainties
(9 i n the calls in kHz
f
Transient duration
Carrier frequency
Male opening semisyllable
Male closing semisyllabk
Female closing semisyllable
2
8
7
18
17
4.5
2.3
2.4
Sternpleurus nobrei
Male whole syllable
Female closing semisyllable
2
2
15
17
7.5
8.5
Sternpleurus stali
9
ACOUSTIC BEHAVIOUR IN S7EROPLEURUS
I65
resolving particular transients. Further Stephen & Hartley (1991) found that the
resonant frequency of these transients (the carrier frequency) was the only part
of the call to be transmitted over any distance. The behavioural responses of
these two Steropleurus species further support the idea that the carrier frequency is
the principal component in acoustic communication and that this type of insect
can in some way resolve it, as clearly shown by Rossler el al. (1990).
Conspecific males and females were able to react acoustically with one another
in noisy environments, implying that they could resolve their species’ calls even
when contaminated by other sounds. This further supports the idea of the
importance of frequency resolution.
Young adult females did not respond to the calls of males of the other species,
but old females were observed occasionally to reply to other tettigoniid calls such
as Ephippiger ephippiger. The Ephippiger males were also quite old and therefore
would have been producing a call encompassing a wide range of frequencies,
caused by the roughness of the worn file teeth (Hartley & Stephen, 1989). The
observed response could also be due to failing discriminatory ability in old, matedeprived, females.
Other features of the calls appear to be unusable for various reasons. For
instance the tooth strike rate ( > 1000 Hz) is too fast to be resolved, and hence
the number of teeth struck, cannot be counted, except perhaps in the major
syllable of S. nobrei. The tooth strike rate itself is not constant and therefore will
not generate its own distinctive frequency. Further, Stiedl, Bickmeyer &
Kalmring (199 1 ) showed that Ephippiger ephzppiger were unable to discriminate
tooth impact intervals varying within k 1 ms of the normal rate of 1/1.87 ms.
Pulse or syllable lengths or intersyllabic intervals seem to be too variable and
also could be confused by overlapping echoes.
Syllable number is too variable with too much overlap between the species to
have any separative value. The same is true of the syllable repetition rate. The
major syllable of male S. nobrei is obviously quite distinctive. O n this basis one
could have a sort of code of pulses. However, the variability in form of the female
replies, on which the male performs phonotaxis, does not support such an
argument. A third species of this group S. ortegai also produces a long
terminating syllable (Hartley, personal observations; Heller, 1988) so reliance on
pulse coding could again lead to confusion.
A reply falling within a specific time window is a very important aspect of
species recognition and consequent phonotaxis in phaneropterine bush-crickets
(Robinson et al., 1986; Heller & von Helverson, 1986). If time windows are
involved with these two Steropleurus species, then they must be rather wide.
Females of both species have been observed to start replying before the end of the
male call, and yet on other occasions to have a delay of up to 400 ms. The
type B, or long call, of female S. nobrei may be up to 3 s later. With a long delay
it is possible for the female to identify the call before replying rather than
responding with a more or less reflex action as seems to occur in the
phaneropterines. Even where the call and reply overlap, the male call is
sufficiently long for some features to be identifiable before the female starts to
respond. Further support for the idea of some time window is the fact that there
was no evidence of males performing phonotaxis on female replies generated in
response to other males’ calls. It is also unlikely that females need to receive and
identify a number of male calls before they start to reply, since male calls will be
I66
J. C. HARTLEY
rather infrequent if no reply is forthcoming. The secondary song in S. nobrei may
also be part of a time-related recognition pattern.
Once a duet is established, phonotaxis can be performed by either or both
partners. In general males seem to be faster and more accurate than females. In
mate-deprived laboratory studies, males contribute about 70% of the approach
movements. Females often seem to stop short of a male and may even move
away, followed by the male.
Phonotaxis by either sex on the call of the prospective mate extends the range
of known phonotactic interactions in bush-crickets given by Robinson (1990).
They were; (a) the reiteratively calling male attracting a silent female; (b) the
sporadically calling male, a responding female, whose replies stimulate a n
increased call rate from the male, whereupon the female performs phonotaxis;
(c) a calling male and responding female with the male performing phonotaxis
on the female reply; there is now (d) a calling male and replying female with
either or both partners moving. So far there is no evidence of a situation where
the female initiates calling. It is possible that the type B (long) reply of S. nobrei
could be a step in this direction, but at present it is only produced in response to
a male call. However, such a strategy would seem unlikely. If calling is a costly
and dangerous process and the female with her egg load is the more vulnerable
sex, then selection for a 'low profile', only producing sound and moving little
when stimulated, would be favoured. Against this one must wonder why it is
only in the Phaneropterinae and Ephippigerinae that these systems have
evolved, and that in the rest of the Tettigoniidae the male calls and female moves
(see Robinson, 1990 for further discussion on this subject). At present it is not
possible to say whether the behavioural pattern exhibited by these Steropleurus
species is a more or less highly evolved system within the Ephippigerinae,
although my own feeling is that it is more advanced.
ACKNOWLEDGEMENT
I would like to thank Paul Cunningham for the hours spent in observing and
recording the behaviour of these insects.
Note added in proof
Since going to press it has transpired that this population of Steropleurus nobrei is
indistinguishable, both acoustically and morphologically, from specimens
collected by Mr J. Reynolds in the same region as the type locality for
S. asturiensis (Bolivar) and identifiable as such. As the type locality for S. nobrei is
further south in the Serra da Estrela there is a strong possibility that the species
referred to in this paper as S. nobrei is really S . asturiensis and that the given
distribution of S. nobrei including the Picos (Harz, 1969) is incorrect, or that the
two names are synonymous.
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