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Underwater stridulation by corixids: Stridulatory signals and sound producing mechanism in Corixa dentipes and Corixa punctata
J. Insect Physiol. Vol. 29, No. 10, pp. 761-771, Printed
1983
in Great Britain
Copyright
0
0022-1910/83 $3.00 + 0.00 1983 Pergamon Press Ltd
UNDERWATER STRIDULATION BY CORIXIDS : STRIDULATORY SIGNALS AND SOUND PRODUCING MECHANISM IN CORIXA DENTIPES AND CORIXA PUNCTATA JOACHIMTHEISS,JOACHIMPRAGER and RICHARD STRENG Institut fiir Zoologie, UniversitltsstraDe
3 1, D-8400 Regensburg, Federal Republic of Germany
(Received 15 February 1983 ; revised 25 April 1983)
Abstract-(l) The species-specificsongs of Corixa dentipes and Corixa punctata males are composed of pulse trains, each of which contains about eleven sound pulses. C. dentipes has a repertoire of four different songs (Song A-D). These songs differ in overall duration, pulse-train repetition rate, and amount of variability in pulse-train rate, pulse rate and sound intensity during the song or individual verses. C. punctatu produces only one song. Its sound pattern is considerably more variable, even for an individual animal, than the very precisely performed C. dentipes songs. (2) In the case of C. dentipes, the highest measured peak sound pressure level (SPL) of single pulses was 133 dB re 1 @a at a distance of 0.1 m from the animal, and the mean of the largest pulses per pulse train over the entire Song A was 115 dB. The song of C. punctutu is less loud, with a SPL ca. 1&20dB lower than that of the C. dentipes songs. The measurements permit estimation of the alternating pressures at the thoracic tympanal organs during acoustic communication. (3) The stridulatory apparatus consists of two specialized structures. The file (pars stridens) is a field of ca. 20 parallel rows of thickened bristles (pegs) on the femur of each foreleg. There are distinct species- and sex-specific differences in the spacing of the rows and the thickness of the pegs. The counterpart of the file, the maxillary plate or scraper (plectrum), is a specially thickened cuticular projection on the side of the head. (4) A single downstroke of the file over the scraper produces a train of acoustic pulses. Each pulse is associated with the contact between one row of pegs in the file and the scraper. Structure and movement of the stridulatory apparatus indicate that at most three adjacent pegs in a row contact the scraper to generate a single pulse. (5) The foreleg movements during various songs can be unilateral, alternating or synchronous. Results indicate that even when the two forelegs move in synchrony the sounds are produced by only one leg, so that in general superposition of stridulatory pulses is avoided. The speed of the downstroke, the repetition rate of consecutive leg movements and the duration of stridulation are temperaturedependent. The Qlo for the pulse-train rate is between 2.7 and 2.0 for water temperatures between 4°C and 25°C. Key
Word Index:
Sound signals, sound production,
acoustic communication,
aquatic
insects,
temperature-dependence
INTRODUCTION The sounds that corixids produce by stridulating under water have been described for various species (Jansson 1973, including a summary of earlier findings, 1976, 1979a,b; Schulze 1977; Aiken 1982). Corixa punctata and C. dentipes are particularly interesting objects for research on the stridulatory sounds and their production, for several reasons. (1) The two species live sympatrically in Central Europe, and at least in southern Germany they are also syntopic. (2) They use the same frequency band for their acoustic signals (TheiD, 1982). If these signals are significant in species isolation-as has been shown for the genus Cenocorixu (Jansson 1973)-then their song repertoires would be expected to show speciesspecific differences. (3) The two corixid species studied here are the only ones for which quantitative data on the mechanical and physiological properties of the thoracic tympanal organs are available (Prager 1976, Prager and Larsen 1981, Prager and Theil3 1982, Prager and Larsen in preparation). The tympanal
membranes of these organs are in direct contact with the bubble of respiratory air that constitutes the physical gill, which covers large areas of the body surface of submerged corixids. The air bubble plays a central role in sound production and sound reception by corixids (TheiD 1982, Prager and Streng 1982). The morphological findings and cinematographic analysis of stridulatory movement presented here offer an explanation of the way the frictional forces acting on the exoskeleton could be converted to pulsations of the sound-radiating air bubble. Quantitative data on intensity of the stridulatory signals of C. punctatu and C. dentipes provide the first opportunity for calculating the sound pressures developed within the air bubble of water insects-that is, immediately adjacent to the auditory organ-during acoustic communication. ANIMALSAND METHODS The animals were caught in the field (Oberpfalz, Bayem) in various ponds ; the different species (identi751
JOACHIM THEM it cd
762
fied by reference to Stichel 1935) were kept separately in a concrete basin in an atrium of the University of Regensburg or in 60 I aquaria. Our observations were carried out over a period of more than two years. A permanent record of the stridulatory activity of 1O-20 males of each species was kept for the life of the animals and was displayed with a pen-writer. To be certain that individual animals can perform the entire song repertoire of the species, control experiments were done with individuals. The temporal pattern of the stridulatory sounds was examined by display on a storage oscilloscope or on films of oscilloscope traces. The tape recordings (Nagra IV-SJ) used to determine the SPL of the pulses in the songs were obtained in a “natural” corixid habitat in the field. The hydrophone (Briiel and Kjaer, Type 8101) was positioned 0.08 m below the water surface, with the animal 0.1 m below the hydrophone and ca. 0.4 m above the muddy bottom of the pond. The distance from shore was about 1 m. Throughout the text the SPL given for an individual pulse is the maximal peak SPL of the pulse re 1 PPa. With the arrangement used here, reflections from the water surface can introduce an increase of at most + 2 dB. The stridulation movements were filmed with a high-frequency camera (Hycam; 16 mm, 96 and 190framesis). The sounds were recorded simultaneously on a stereo tape recorder (Revox, A77) using a hydrophone, conditioning amplifier and measuring amplifier (Briiel and Kjaer, Types 8103. 2650.2607). Sound and picture were synchronized by a voltage pulse from the camera, recorded on the second track of the tape. During filming the animal was kept in a small glass cuvette.
RESULTS
Strwturr
(?I’the .stridulutory upparatus
The legs of submerged corixids project out of the ventral air bubble into the surrounding water. On the bases of the femora. there is a water-repellent field of hairs that forms the boundary between the air bubble and water. On the fore femora of Corka some of the hairs are conspicuously thickened at the base; these pegs are arranged in about 20 parallel rows (Fig. lc). The joint between peg and cuticle is set at an angle so that the pegs point distally, and the base of the peg is surrounded by an asymmetrical socket. There are significant differences in thickness of the peg base, both between C. punctafa and C. dentipes and between the two sexes of each (Fig. 1, Table 1). The distance between neighbouring pegs in a row is 25535pm in the male. The rows themselves are closer together proximally than distally; their mean separation is given in Table 1. These fields of pegs on the fore femora of the males act as a file (pars stridens) during stridulation. In some cases the pegs were found to be worn down in a way that would correspond to this use of the structure (Fig. lc). The limited extent of the worn area indicates that a certain part of the field is used preferentially for stridulation or is particularly exposed to friction. Like other corixids. Corha has a projecting maxillary plate that forms a sharp ridge on the side of the head below the antenna. Its dimensions are similar
in both species and sexes, with height ca. 35 kern and length ca. 100 pm. As Jansson (1972) found in Cenocori.xu, this ridge serves as a scraper (plectrum), against which the file rubs during stridulation. In the typical resting posture, corixids hold on to the substrate only with the middle legs; the swimming legs are stretched out to the sides. Starting from this position-or in a few cases while swimming-the males begin to stridulate by moving the forelegs forward and down so that they pass diagonally over the side of the head. The sound signals are produced when, in the course of this movement, the file is rubbed across the scraper, “against the grain” of the pegs. This kind of sound production appears to be typical of the Corixinae (Jansson 1972). We shall describe the stridulatory sounds first as the stridulation movements differ in some of the various songs. The stridulatory sounds Here the term “stridulatory sound” refers only to the sounds produced by the typical stridulation movement of the forelegs. Other sounds made by the animals-for example. during cleaning, diving and copulation-are not treated here. In accordance with the nomenclature suggested by Broughton (1963) and adopted by Jansson (1973) for corixid songs, the song repertoire of various species consists of one or more songs, each of which can consist of one or more verses (Fig. 2). The songs are composed of several distinct pulse trains (Fig. 2d,e). The individual pulses in a train are resolved in Fig. 2e; the time course of the single pulse has been described elsewhere (TheiD 1982). We shall refer to the mean of the peak amplitudes of the pulses within a pulse train as the pulsetrain amplitude. The song repertoire
of C. dentipes
A population of male C. dentipes routinely produces four clearly distinguishable songs. Because their biological significance is not yet clear, they will be designated here by the letters A, B, C and D. Isolated individual animals are capable of singing all four songs. The most important data are summarized in Table 2. Song A (Fig. 2a). The song begins relatively faintly, with alternately higher and lower pulse-train amplitudes. This initially alternating rhythm usually persists only for the first quarter of the song, after which it gives way to an irregular sequence of loud pulse trains with a few faint trains interspersed. On the whole the intensity of the sound increases up to the middle of the song and then decreases toward its end (Fig. 2h). The pulse-train repetitionrate is roughly constant over Table 1. Diameter of peg base and distance between peg rows in C. dentipes and C. punctnru. in the middle of the file. Means +SD for 20 individual measurements of at least 5 anjmals Peg diameter (m) C. denripes ,J C. punctata J C. dentipes i c. punl’mtcr +
13.1 kO.1 7.7 f 0.8 8.2 k 1.0 3.8 f 0.3
Row distance (mrm) 51.5 40.0 38.0 20.7
+ 3.6 t4.6 k 3.2 & 4.0
Fig. I. Thickened bristles (pegs) in a C. punctatumale (d) and female right foreleg. The arrows in (c) are are worn down more than others. fronto-lateral
the middle of the file of a C. dentipes male (a) and female (b) and (e); (c) entire file of a C. puncrutamale. cx coxa, fm femur of the aligned with a row of pegs; note that some of the pegs in the file f-h scraper (arrows) on the right side of the body, as seen from (f), ventro-lateral (g) and along its ridge (h).
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Sound
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the entire duration of the song. The ratio of pulse-train duration to the duration of the pauses between consecutive pulse trains is about 1 : 1. Sometimes additional brief low-amplitude pulse trains (l-3 pulses) appear within the pauses (arrows, Fig. 2a). Song B. With only a few exceptions, the song consists of a sequence of several similar verses separated by brief pauses. This song is usually followed immediately by Song C (B + C, Fig. 2h). A verse of Song B typically has a fairly faint beginning and a louder pauses
ending (Fig. 2b). During the initial part the between the pulse trains can become very brief
or be entirely eliminated. Often an isolated pulse train near the beginning is exceptionally loud (arrows, Fig. 2b). During the louder final part, the number of pulses per train is distinctly lower than in the initial part or in Song A. In the extreme case only 1 pulse per “train” is produced. Accordingly, the pauses between the pulse trains are longer than in the initial part. The pulse-train rate of a verse of Song B is significantly higher than that in Song A. When several verses of
7Gmx
h
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by Corixids
165
Song B are sung in succession, the pulse-train rate and the intensity rise progressively. Song C. Normally C is sung as a continuation of Song B. Although the two songs closely resemble one another in structure, they are presented separately here because one is frequently sung without the other. The initial part of C corresponds to a continuation of Song B except that there are no pauses between the verses (Fig. 2h). Pulse-train rate and intensity continue to increase in each successive verse until Cm,, (Fig. 2~). In the subsequent final part, verse C,,d, the song dies away. The pulse-train rate of Ce,d corresponds to that of Song A, being only half as high as in C max. The repetition rate of the pulses within a train is correspondingly lowered (Fig. 2e). Song D. This song is sung less commonly than the others (TheiD in preparation). In structure it resembles Song B + C (Fig. 2h), in that D too is composed of a sequence of similar verses at progressively increasing intensity and gradually dies away in the final part. But the pulse-train pattern of the individual verses is
--Cend
10s
n
Fig. 2 a-f. Oscillograms of the stridulatory sounds of C. dentipes males: a initial part of Song A; b two verses of Song B; c two verses of Song C and initial part of verse Cend; d transition from C,,, to Cend (section taken from c); e last pulse train of C,, and first pulse tram of C,, (section taken from c): f two verses of Song D. g Two verses of the song of C. punctata males. h Typical time course of complete songs after rectification and integration for recording on a pen-writer. Arrows: see explanations in text. For analogy with other songs, Song B is defined somewhat differently here than by TheiD (1981).
166
JOACHIM THEISS et al. Table 2. Quantitative description of the songs of male C. dentipes and C. punctata. 1st column: means + SD of 10 complete songs in each case. 2nd and 3rd columns:
except for Song A the data refer to the middle part of the verses, in the case of Song C to Cmax: n = 20. Water temperature 12-l 5°C
Duration of the song (s)
Number of pulses per pulse train
B c
21.9 + 4.0 77.0 t 9.3 66.7 f 6.9
10.8 +_2.5 11.7 f 1.0 11.4 + 1.4
D C. punctata
84.7 ? 11.5
11.9 +0.7
47.5 k 7.0
10.8 + 1.0
Pulse-train rate (pt/s)
C. den tipes A
much less regular than in Songs B and C. It is typical of the individual verses in D that 34 pulse trains are especially emphasized (arrows, Fig. 2f). Moreover, the song is fainter than B $ C. The song of C. punctata
Although the stridulatory sounds of this species were monitored regularly over a 2-year period, only one type of song was recorded. It differs from songs of male C. dentipes; of the four, it resembles Song D most closely, but it is significantly shorter (Fig. 2; Table 2) and on the whole fainter. As in Song D of C. dentipes, occasional pulse trains within a verse are emphasized (Fig. 2g). When the stridulatory sounds of the two species are compared, it is striking that C. puncfata males produce considerably less predictible sound patterns. Often no specific pattern is detectable, and the song cannot be subdivided into a sequence of similar verses. Soundproducing
4.3 * 0.4 6.7 + 1.0 8.6 + 1.0 Gl,,) 4.7 f 0.3 4.8 +0.3
C. dentipes males the mean distance between the 11 rows of pegs in the middle of the file area is about 46 pm. Therefore when the direction of motion is such that the scraper moves almost perpendicular to the peg rows the mean repetition rate of the pulses in a train would be ca. 150 pulses/s. It can readily be calculated from the data in Table 1 and Fig. 5 that the measured pulse rate in a train averages ca. 140 pulses/s, which is approximately consistent with the prediction. Each sound pulse corresponds to one row
mechanism
To reveal in greater detail the relation between leg movement and sound pattern, C. dentipes males were filmed while producing Song A and the stridulatory sounds were synchronously tape-recorded. Singleframe analysis gave the following results. In the examples of Figs 3 and 4, the left leg is moved up and down at about twice the rate of the right leg, with no clear phase relation between the two (Fig. 4). The downstroke of the leg is slower than the upstroke. Only during the downward movement of the left leg is a pulse train produced (Fig. 3). The phase relation between the movement of the left leg and the production of a sound is within the resolution permitted by the frame rate (Fig. 4). It was also evident in the film that the right leg is not held as close to the head as the left leg. In a given individual the right Ieg can have the more rapid rhythm during some renditions of Song A and the left leg during others. The same movements are also observed at lower water temperatures. It is very likely, therefore, that Song A is produced with only one leg. At each movement of the file over the scraper a pulse train is produced; thus the pulse-train rate of Song A corresponds to the rhythm of the more rapidly moving leg. The velocity v with which the file moves over the scraper can be estimated from the films. During the performance of Song A at 2O”C, v is ca. 7mm/s. In
Fig. 3. Movements of the right (0) and left (0) forelegs of two C. dentipes males during two phases of Song A (a initial segment, b middle segment). Above each graph is an oscillogram of the synchronous record of the sound. At the bottom is a scale showing the timing of the consecutive frames of the films (96 frames/s), with drawings of every third frame for (b). Ordinate: distance of the femur-tibia joint, in the plane of the picture, from an intermediate position ( = 0). Water temperature 20°C.
161
Sound production by Corixids
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or, a b
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7
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c
d
Fig. 4. a Time difference between the highest point of the leg movement (right A., left 0) and the middle of the next pulse train, for a section of Song A of a C. dent&es male. b Up-and-down movement of the right leg and c of the left leg. d. Oscillogram of the song. Data obtained from films as in Fig. 3.
of pegs moving across the scraper. Comparison of the size of the scraper and the distance between the pegs (Fig. 1) shows that the scraper encounters at most 3 adjacent pegs in a row on each passage. Observation of the stridulation movements at low water temperature was sufficient for describing the movements in the following songs. Unlike Song A, Song B is produced by alternating movements of the two legs, a pulse train being produced by each downstroke. During the louder terminal part of each individual verse the fore femora are held at a steeper angle. The same is true of Song C up to the verse C max. In the subsequent verse C,,,. as the song fades away, the pulse trains are produced by only one leg; the other is hardly moved. Because the soundproducing leg continues in the same rhythm as during Cma: the pulse-train rate is halved. Surprisingly, the pulse repetition rate within each train is also reduced (Fig. 2d,e). This finding indicates that during this verse the downstroke of the sound producing leg is slower than during C,,. As in Song B, the first part of each verse of Song D is produced by alternating movements of the two legs. In the middle of the verse the rhythm changes ; one leg is held at a steeper angle and the other stops stroking briefly. The final part of D, like Cen& is performed with only one leg. The sequence of. leg movements in stridulating C. punctuta males is like that in Song D of C. dent&s males but considerably more variable. Influence of temperature on the stridulation movements
Both the repetition rate of the sequence of leg movements and the velocity of each movement depend on temperature. As a result, the pulse-train rate and the pulse rate within a train depend on the temperature
of the water. The influence of the water temperature on the pulse-train rate was examined quantitatively for Songs A and C of C. &wipes males between 4 and 25°C. Qn a semilogarithmic plot (Fig. 5) the data depart slightly but distinctly from a straight line, indicating that in the range of temperatures studied Qio is not constant. For Song A the QiO in the range 414°C is 2.7, whereas in the range 15-25°C the QiO is 2.0. At temperatures above 20°C only Song A is performed. The pulse-train rate of C,, is always twice that of Song A and of Cend, regardless of the temperature. Taking into account that the precision of the temperature measurements is no greater than a 1°C the scatter of the data is very slight; the standard deviation for Song A and Cend is + 0.3 pt/s, independent of + 0.2 pt/s and for C,,,, temperature. The influence of the temperature on the duration of stridulation varies among the different songs (Table 3). Song A is shortened much more at higher temperatures than is the song combination B + C. This effect is only partially due to the fact that at higher temperatures a larger number of B verses are sung before the transition to C. Whereas the total number of pulse trains in Song A-and thus the number of downstrokes of the stridulating leg-is about the same at 5°C as at 20°C the number of pulse trains in Song B + C is about doubled. There is no significant influence of temperature on the ratio of pulsetrain duration to pause duration. The pulse rate within a train exhibits the same temperature dependence as the pulse-train rate. Soundpressure level (SPL) of the stridulatory sounds The SPL values for the largest pulse per train, averaged over complete songs (SPL,) of males of three corixid species, are shown in Table 4 together with the largest measured single values. The SPL, for the verse C maxof C. dentipes is about 10 dB higher than that for Song A. The singing of C. dentipes, then is
1
0
5
0
15
20
oc
, 25
Lo
Fig. 5. Pulse-train rates (log scale, left ordinate) of Song A (0) verse C,, (D) and C,,,(A) as a function of water temperature. Means of 20 individual measurements of long sections of the songs of 5 C. dentipes males. For comparison, data of Song A (0) &SD with a linear scale (right ordinate.)
768
JOACHIM
THEISS
et
al.
Table 3. Temperature dependence of the songs A and B + C of C. denfipes males, for the water temperatures 5 and 20°C. T. mean overall song duration at 5 ‘C (T,) and 2O~C (T,), for 20 songs in each case; pulse-train rate of Song A from Fig. 5 5C Song A Duration Pulse-train Pulse rate
rate
Song B -1 C Duration Pulse-train rate Number of verses
about
T, - 74 t 10.6 s 1.8ptjs 40 p/s T, - 190 k45.7 2.9 pt/s 9.0 + 2.9
10-20 dB louder than that of C. punctata
Callicarixa
20 c
and
praeusta.
Because of the marked fluctuation in intensity of the pulse trains, especially in Song A (Fig. 2a). the percentage distribution of the highest SPL in the measured pulse trains is shown as a histogram with 5-dB class width in Fig. 6. The distribution has a maximum that coincides roughly with the mean SPL,. About 90% of the values are above 100 dB re 1 @a. When one animal in a population of C. dentipes males begins to sing Song A, often one to several conspecifics join in the song (choral stridulation). The SPL, of such choral stridulation is higher by 3.5 dB than that found for individual animals (Table 4). Accordingly, relatively high pulses occur more frequently during choral stridulation than during individual songs (Fig. 6). This observation can be explained by summation of single pulses produced by different animals (c.f. also Finke and Prager 1980). It remains to be learned whether individual animals also intensity during choral increase their sound stridulation. For one typical Song A the SPL of each pulse was measured. Fig. 7a shows the distribution of pulse amplitudes in the song. They are not normally distributed, because the song begins with a fainter section and also dies out gradually. Within a pulse train, the pulses near the middle have higher amplitude on the average (Fig. 7b).
Comparative
aspects
4.5
T, = 16 f 2.2 s 7.1 pt/s 140 p/s s
T, = 114 k34.8 10.7 pt/s 14.5 f 5.0
s
1.7
Table 4. Peak SPL of the largest amplitude pulse in each pulse train, averaged over 10 complete songs in each case + SD (SPL,). and the largest single value obtained (SPL,,,), in dB re 1 pa. Distance from animal 0.1 m. In choral stridulation 2-4 animals sing simultaneously SPL, C. dentipes (Sow A) Single Chorus c. punctntu Call. praeusta
115.0 118.5 105.4 107.2
SPL,,,
k4.4 +2.7 f 4.4 * 3.3
133dB 119dB 117dB
With regard to the temporal structure of the songs, only Song B + C differs distinctly from all the other songs; the pulse-train rate is significantly higher and rises during the song, while the number of pulses per pulse train becomes smaller at the end of each verse. The differences among the Songs A and D and the song of C. puncrata lie in their duration and intensity modulation. According to Jansson (1973), stridulatory
30 % 26
DISCUSSION
T,/T,
1
22
al‘ carixid sound signals
There are distinct differences between the sounds produced by male C. dentipes and C. punctata. The most conspicuous of these are (1) the extensive repertoire of C. dentipes as compared with the single song of C. punctata, (2) the greater precision in the stridulatory pattern of C. dentipes as compared with the variability, even within an individual, of the sound patterns of C. punctata, and (3) the lo- to 20-dB higher intensity of the C. dentipes songs. It can be concluded from these differences that a species-specific sound pattern is far more significant for C. dentipes than for C. punctata. This conclusion is supported by the observation that the stridulation and reproductive phase of C. punctata begins some months prior to that of the competing C. akntipes (TheiB 1981).
6
106
113
118
123
1
Fig. 6. Distribution (in 5-dB classes) of the peak SPLs of the largest pulse per pulse train in 10 complete examples of Song A from various individual animals (shaded columns) and in 10 choral songs (white columns; 24 C. dentipes males singing simultaneously); dB re 1 @a, 0.1 m from animals to hydrophone.
Sound
production
769
by Corixids
1
111 b dB
107
1
20-
!
16-
103-
i
12-
0-
9496
99. 103
N)4106
109. 118 114- ;$-dB 113
95-i,, 12
I
4
I
,
6
,
I
8
I,
10
I
I,
12
N
I 14
Fig. 7a.b. Peak SPL of all the pulses in a typical Song A that exceed 89 dB re 1 pa (0.1 m from animals to hydrophone). a Distribution of the peak SPL of all the 732 pulses in the song, in 5-dB classes. b Peak SPL of the Nth pulse in a pulse train, averaged over all the 79 pulse trains in the song &SE (standard error). The numbering of the pulses was centered on the middle of the pulse train, the number N = 7 being assigned to the middle pulse in each case. Because the number of pulses per train varied between 3 and 14, the means were calculated from varying numbers of single values (n) (smallest n = 28); pulses numbered 1,2 and 14 were so rare that no mean was calculated.
sounds of the genus Cenocorixa serve as a premating isolation mechanism. In this genus, pulse rate and pulse-train rate evidently play a subordinate role in specificity, for there is extensive overlap of these features among the various species (Jansson 1974). In the Orthoptera the syllabic pattern of the songs (a syllable is equivalent to a pulse train), and in some cases the amplitude modulation of the single syllable, is crucial for recognition of the conspecific signal (review by Elsner and Popov 1978 ; von Helversen 1979; Weber et al., 1981; Thorson et al., 1982; cf. also Gogala 1970 for Cydnidae). Schulze (1977) described only one type of song produced by male C. dentipes. His published data on the structure of the song indicate that it was the one here called Song A. He could not observe the other songs because in his experiments the water was kept at a constant temperature of 22°C; our own observations show that at temperatures above 20°C only Song A is sung. As in other corixids (Finke 1968; Jansson 1974), the pulse-train rate of C. dentipes song rises with increasing water temperature. Because the Qio becomes smaller at higher temperatures, this relation cannot be described by an exponential function. Such a decrease of the QiO with rising temperature corresponds to the Arrhenius equation of thermodynamics, and appears to be demonstrable for all movement sequences of poikilothermic animals as long as the range of temperatures tested is not too small. Walker (1975) has proposed a linear model to describe the temperature dependence of movement cycles of poikilothermic animals, and has documented such linearity for the wing-beat rate of stridulating orthopterans. Over the entire 21°C temperature range studied, the temperature dependence of the pulse-train rate of C. dentipes departs distinctly from linearity (Fig. 5). This is also the case for some species of Cenocorixa (Jansson 1974). Comparison of the correlation coefficients of the linear and exponential regression curves as done by Walker (1975) does not seem to us to be appropriate here,
measured here obviously lie between an exponential and a linear function (see Fig. 5). Data on the sound pressure levels (dB re 1 pa) generated by stridulating corixids are available for several species : Sigara striata (122-125 dB at a distance of 0.12-O. 15 m from the animal) and Callicorixa praeusta (102-108 dB, Finke 1968) Corixa dentipes (101-l 11 dB, Schulze 1977), and Palmacorixa nana (11 l-124 dB, Aiken 1982; 100 dB must be added to the values 1l-24 in Aiken 1982 (Aiken personal communication)). All these measurements were done in small containers, and in no case is it stated whether the peak SPL of single pulses is meant. According to our observations, S. striata stridulates about as loudly as C. dentipes. Therefore Finke’s data probably refer to the peak SPL actually produced. Sound-intensity measurements we did as a control on Callicorixa praeusta (Table 4) confirm Finke’s results. Schulze estimated the loudness of the C. dentipes songs by the fact that the stridulation was just barely audible outside the aquarium. His estimate is about 1&20dB lower than the values we measured. The dynamic range of 18.5 dB given by him is incomprehensible; with an A-weighted background noise < 70 dB in our measurements, the range of pulse amplitudes produced by C. dentipes amounts to ca. 60 dB (Table 4). since the data
Estimation of the sound pressure level at the tympanal organs
Sound radiation in corixids is brought about by volume pulsations of the respiratory air bubble of the physical gill, and a spherical air bubble can be used to first approximation as a model of this emitter (Then3 1982). For an air bubble oscillating underwater at its natural frequency such as to generate an SPL of 131 dB re 1 $a at a distance of 0.1 m, it can be calculated that the radius changes by Ai = 0.8 m (Eq. (l), Appendix). It follows that the maximal oscillation amplitudes of the air-bubble surface of a stridulating animal can be estimated at a few nrn.
770
J~ACHIM THEISS et al.
The threshold curves of the thoracic tympanal organs, in contact with air even in submerged corixids, have been measured with airborne sound for C. punctata (Prager 1976; Prager and TheiB 1982). Until now, alternating pressures which occur within the air bubble of submerged corixids during acoustic communication have been unknown. It therefore appeared particularly interesting to estimate the alternating pressures in the air bubbles of a stridulating animal and in that of a listening animal some distance away, by means of the air-bubble model (see Appendix). The calculations indicate that the pressure within the air bubble of a stridulating animal is ca. 36 dB above the SPL measured 0.1 m away. For a stridulating C. punctata male, then, even the low-intensity stridulatory pulses would be above the threshold of those sense cells in the thoracic scolopale organs that have so far been studied. On the assumption that the average resonance step-up of the sound pressure entering the air bubble of a listening animal is ca. 1OdB (Prager and Streng 1982, TheiB 1982), the mean SPL for the largest pulse in each pulse train of the C. punctata song would be 115 dB within the bubble of a listening animal at a distance of 0.1 m from the singer (Table 4). This means that even at this short distance the entire pulse pattern of the song-including the low-amplitude pulses ,in the train-can be transmitted only by the more sensitive sense cell (Al) in the mesothoracic tympanal organ. If the distance between a singing and a listening animal is still shorter the two animals must be considered as coupled oscillators (c.f. Meyer and Skudrzyk 1953). Soundproducing mechanism The SEM pictures of the file reveal
distinct sexspecific and species-specific differences in the thickness of the stridulatory pegs. In the males the thickness of the pegs is positively correlated with the intensity of the stridulatory sounds. Jansson (1972) found a similar relation in Cenocorixa. Because the stridulatory pegs of C. punctata males are equal in thickness to those of C. dentipes females, one might suspect that in C. dentipes the females are also capable of stridulation. As films and direct observations of stridulation movements indicate, the two forelegs do not simultaneously produce sound in any of the songs of C. dentipes and C. punctata. The contradictory statement by Schulze (1977) should be considered with caution because his observations were made at room temperature with the unaided eye. Although, synchronous downward movements of the forelegs can occur (Fig. 3a), the present results corroborate Jansson’s (1979b) view that in the Corixinae the two legs do not actually produce sound simultaneously. In exceptional cases, when the legs are alternating, the end of one pulse train can overlap the beginning of the next in some songs. Unlike the songs of acridid grasshoppers (Elsner and Popov 1978), the sound patterns of the Corixinae, thus usually consist of distinct pulses and pulse trains, produced by a single leg. The conclusions about the sound-producing mechanism to be drawn from these results are as follows. From the direction of foreleg movement during stridulation and from the structure of the stridulatory apparatus it must be concluded that the pegs in the file with their thickened bases touch only the scraper;
that is, it is not a matter of an entire row of pegs sweeping in a broad front over the side of the head, as in the descriptions of Finke (1968) and Schulze (1977). From the dimensions of the scraper and from the size and separation of the pegs it follows that 1 to 3 adjacent pegs per row catch on the scraper. Because the pegs are seated in the cuticle in such a way that during the downstroke they are inclined toward the approaching maxillary plate, they are especially likely to hook over its sharp edge. The forward movement of the femur drags the head along until the scraper slips off the row of pegs (c.f. Aiken 1982), allowing the head to swing back into its starting position or until the scraper catches in the next row. When it is suddenly released the head, which covers a large area of the animal’s air bubble like a cap, thereby transmits an impulse to the air bubble that sets off volume pulsations of the bubble at its natural frequency. In this way a sound pulse is produced. The weaker pegs in the file of C. punctata displace the head less before it slips off, so that the restoring force is less and the stridulatory signals are not as loud. This explanation of the mechanism of stridulation is supported in principle by studies of the frequency spectrum of the stridulatory pulses and the way the oscillations are damped (TheiD 1982). Acknowledgements: We thank Professor Dr D. Burkhardt and Dr I. Veit for critically reading the manuscript, Miss Helga Vi5lkl for technical assistance and the Deutsche Forschungsgemeinschaft for financial support (SFB 4, Regensburg). APPENDIX I. Let us assume a spherical air bubble under water with volume V, at rest exhibits volume pulsations V, at its natural frkquency o,, (V, = V, + A 3; sin w,, I; A P, 4 V,; cf. TheiD 1982). How large is the radius change Ai, of the pulsating air blbble, if it-produces a sound pressure pl at distance I from the centre of the bubble (2 means peak value of x)? According to Strasberg (1956) the radius change is given by A;,
=
!!!L
3KP where an adiabatic exponent H = I .41 and p = 1atm can be assumed (TheiS 1982). With a peak SPL of 131 dB re 1 PPa at distance I = 0.1 m one obtains A;, = 0.8 pm. 2. How high is the alternating pressure pulsating air bubble in the above case? According to Poisson’s law
pL within
the
By applying Eq. (1) one obtains 6,/b, = (A P,/Ai,) (1/3 Vol. With Ap,/Ai,-df,/d?, it follows that j$/jj, z l/rO. Given an air bubble with a natural frequency f0 = 2 kHz and hence a radius rO= 1.65mm (c.f. TheiD 1982) one obtains pi/p, u 60. Thus, in this example the alternating pressure with the pulsating air bubble has a 36 dB higher level than the SPL measured at a distance of 0.1 m from the centre of the bubble. REFERENCES Aiken R. B. (1982) Sound production and mating in a waterboatman, Palmacorixa nana (Heteroptera: Corixidae). Anim. Behav. 30, 5461.
771
Sound productic )n by Corixids Broughton W. B. (1963) Method in bioacoustic terminolonv. In Acoustic Behaviour of Animals (Ed. by Busnel RYG.), pp. 3-24, Elsevier, Amsterdam. Elsner N. and Popov A. (1978) Neuroethology of acoustic communication. Adu. Insect Physiol. 13,229-3X Finke C. (1968) LautluBerungen und Verhalten von Sigara striata und Callicorixa praeusta (Corixidae Leach : Hydrocorisae Latr.) 2. Vergl. Physiol. 58,398422. Finke C. and Prager J. (1980) Pulse-train synchronous pair-stridulation by male Sigaru striata (Heteroptera: Corixidae). Experientia 36, 1172-l 173. Gogala M. (1970) Artspezifitlt der LautluBerungen bei Erdwanzen (Heteroptera: Cydnidae). 2. Vergf. Physiol. 70,20-28.
Helversen 0. von (1979) Innate recognition of acoustical patterns and its significance for the isolation of species. Verb. dt Zool. Ges., Gustav Fischer Verlag, Stuttgart, p. 42-59. Jansson A. (1972) Mechanisms of sound production and morphology of the stridulatory apparatus in the genus Cenocorixa (Hemiptera: Corixidae). Ann. Zool. Fennici 9, 120-129. Jansson A. (1973) Stridulation and its significance in the genus Cenocorixa (Hemiptera: Corixidae). Behaviour 46, l-36.
Jansson A. (1974) Effects of temperature on stridulatory signals of Cenocorixa (Hemiptera: Corixidae). Ann. Zool. Fennici II,2888296.
Jansson A. (1976)Audiospectrographic analysis of stridulatory signals of some North American Corixidae (Hemiptera). Ann. Zool. Fennici l&4862. Jansson A. (1979a) Reproductive isolation and experimental hybridization between Arctocortsa carinata and A. germari (Heteroptera: Corixidae). Ann. Zoo/. Fennici 16,89-104.
Jansson A. (1979b) Experimental hydridization of Sigara srriata and S. dorsalis (Heteroptera: Corixidae). Ann. Zool. Fennici 16, 105-l 14. Meyer E. and Skudrzyk E. (1953) Uber die akustischen Eigenschaften von Gasblasenschleiem in Wasser. Acustica 3.434440.
Prager J. (1976) Das mesothorakale Tympanalorgan von Corixa punctata Ill. (Heteroptera: Corixidae). J. Comp. Physiot. 110, 33350.
Prager J. and Larsen 0. N. (I 98 1) Asymmetrical hearing in the water bug Corixa punctata observed with laser vibrometry. Naturwissenschaften 68, 5799580. Prager J. and Streng R. (1982) The resonance properties of the physical gill of Corixa punctata and their significance in sound reception. J. Comp. Physiol. 148,323-335. Prager J. and TheiD J. (1982) The effect of tympanal position on the sound-sensitivity of the metathoracic scolopale organ of Corixa. J. Insect Physiol. 28, 447452.
Schulze M. (1977) Biophysik der Unterwasserlauterzeugung am Beispiel der Ruderwanze Corixa dentipes Thms. Zool. Beitr. 23,477-507.
Stichel W. (1935) Illustrierte Bestimmungstabellen der deutschen Wanzen. Selbstver., Berlin. Strasberg M. (1956) Gas bubbles as sources of sound in liquids. J. acoust. Sot. Am. 28,20-26. TheiD J. (1981) Schallerzeugung und Stridulationsaktivitat bei Corixiden. Mitt. dt. Ges. ANg. Angew. Ent. 3, 235238.
TheiO J. (1982) Generation and radiation of sound by stridulating water insects as exemplified by the corixids. Behav. Ecol. Sociobiol.
10, 225-235.
Thorson J., Weber T. and Huber F. (1982) Auditory behavior of the cricket. II. Simplicity of calling-song recognition in Gryilus, and anomalous phonotaxis at abnormal carrier frequencies. J. Comp. Physiol. 146, 361-378.
Walker T. J. (1975) Effects of temperature on rates in poikilotherm nervous systems: evidence from the calling songs of meadow Katydids (Orthoptera : Tettigoniidae: Orchehmum) and reanalysis of published data. J. Comp. Physiol. 101,5749.
Weber T., Thorson J. and Huber F. (1981) Auditory behavior of the cricket. I. Dynamics of compensated walking and discrimination paradigms on the Kramer treadmill. J. Comp. Physiol. 141, 215-232.
1983
in Great Britain
Copyright
0
0022-1910/83 $3.00 + 0.00 1983 Pergamon Press Ltd
UNDERWATER STRIDULATION BY CORIXIDS : STRIDULATORY SIGNALS AND SOUND PRODUCING MECHANISM IN CORIXA DENTIPES AND CORIXA PUNCTATA JOACHIMTHEISS,JOACHIMPRAGER and RICHARD STRENG Institut fiir Zoologie, UniversitltsstraDe
3 1, D-8400 Regensburg, Federal Republic of Germany
(Received 15 February 1983 ; revised 25 April 1983)
Abstract-(l) The species-specificsongs of Corixa dentipes and Corixa punctata males are composed of pulse trains, each of which contains about eleven sound pulses. C. dentipes has a repertoire of four different songs (Song A-D). These songs differ in overall duration, pulse-train repetition rate, and amount of variability in pulse-train rate, pulse rate and sound intensity during the song or individual verses. C. punctatu produces only one song. Its sound pattern is considerably more variable, even for an individual animal, than the very precisely performed C. dentipes songs. (2) In the case of C. dentipes, the highest measured peak sound pressure level (SPL) of single pulses was 133 dB re 1 @a at a distance of 0.1 m from the animal, and the mean of the largest pulses per pulse train over the entire Song A was 115 dB. The song of C. punctutu is less loud, with a SPL ca. 1&20dB lower than that of the C. dentipes songs. The measurements permit estimation of the alternating pressures at the thoracic tympanal organs during acoustic communication. (3) The stridulatory apparatus consists of two specialized structures. The file (pars stridens) is a field of ca. 20 parallel rows of thickened bristles (pegs) on the femur of each foreleg. There are distinct species- and sex-specific differences in the spacing of the rows and the thickness of the pegs. The counterpart of the file, the maxillary plate or scraper (plectrum), is a specially thickened cuticular projection on the side of the head. (4) A single downstroke of the file over the scraper produces a train of acoustic pulses. Each pulse is associated with the contact between one row of pegs in the file and the scraper. Structure and movement of the stridulatory apparatus indicate that at most three adjacent pegs in a row contact the scraper to generate a single pulse. (5) The foreleg movements during various songs can be unilateral, alternating or synchronous. Results indicate that even when the two forelegs move in synchrony the sounds are produced by only one leg, so that in general superposition of stridulatory pulses is avoided. The speed of the downstroke, the repetition rate of consecutive leg movements and the duration of stridulation are temperaturedependent. The Qlo for the pulse-train rate is between 2.7 and 2.0 for water temperatures between 4°C and 25°C. Key
Word Index:
Sound signals, sound production,
acoustic communication,
aquatic
insects,
temperature-dependence
INTRODUCTION The sounds that corixids produce by stridulating under water have been described for various species (Jansson 1973, including a summary of earlier findings, 1976, 1979a,b; Schulze 1977; Aiken 1982). Corixa punctata and C. dentipes are particularly interesting objects for research on the stridulatory sounds and their production, for several reasons. (1) The two species live sympatrically in Central Europe, and at least in southern Germany they are also syntopic. (2) They use the same frequency band for their acoustic signals (TheiD, 1982). If these signals are significant in species isolation-as has been shown for the genus Cenocorixu (Jansson 1973)-then their song repertoires would be expected to show speciesspecific differences. (3) The two corixid species studied here are the only ones for which quantitative data on the mechanical and physiological properties of the thoracic tympanal organs are available (Prager 1976, Prager and Larsen 1981, Prager and Theil3 1982, Prager and Larsen in preparation). The tympanal
membranes of these organs are in direct contact with the bubble of respiratory air that constitutes the physical gill, which covers large areas of the body surface of submerged corixids. The air bubble plays a central role in sound production and sound reception by corixids (TheiD 1982, Prager and Streng 1982). The morphological findings and cinematographic analysis of stridulatory movement presented here offer an explanation of the way the frictional forces acting on the exoskeleton could be converted to pulsations of the sound-radiating air bubble. Quantitative data on intensity of the stridulatory signals of C. punctatu and C. dentipes provide the first opportunity for calculating the sound pressures developed within the air bubble of water insects-that is, immediately adjacent to the auditory organ-during acoustic communication. ANIMALSAND METHODS The animals were caught in the field (Oberpfalz, Bayem) in various ponds ; the different species (identi751
JOACHIM THEM it cd
762
fied by reference to Stichel 1935) were kept separately in a concrete basin in an atrium of the University of Regensburg or in 60 I aquaria. Our observations were carried out over a period of more than two years. A permanent record of the stridulatory activity of 1O-20 males of each species was kept for the life of the animals and was displayed with a pen-writer. To be certain that individual animals can perform the entire song repertoire of the species, control experiments were done with individuals. The temporal pattern of the stridulatory sounds was examined by display on a storage oscilloscope or on films of oscilloscope traces. The tape recordings (Nagra IV-SJ) used to determine the SPL of the pulses in the songs were obtained in a “natural” corixid habitat in the field. The hydrophone (Briiel and Kjaer, Type 8101) was positioned 0.08 m below the water surface, with the animal 0.1 m below the hydrophone and ca. 0.4 m above the muddy bottom of the pond. The distance from shore was about 1 m. Throughout the text the SPL given for an individual pulse is the maximal peak SPL of the pulse re 1 PPa. With the arrangement used here, reflections from the water surface can introduce an increase of at most + 2 dB. The stridulation movements were filmed with a high-frequency camera (Hycam; 16 mm, 96 and 190framesis). The sounds were recorded simultaneously on a stereo tape recorder (Revox, A77) using a hydrophone, conditioning amplifier and measuring amplifier (Briiel and Kjaer, Types 8103. 2650.2607). Sound and picture were synchronized by a voltage pulse from the camera, recorded on the second track of the tape. During filming the animal was kept in a small glass cuvette.
RESULTS
Strwturr
(?I’the .stridulutory upparatus
The legs of submerged corixids project out of the ventral air bubble into the surrounding water. On the bases of the femora. there is a water-repellent field of hairs that forms the boundary between the air bubble and water. On the fore femora of Corka some of the hairs are conspicuously thickened at the base; these pegs are arranged in about 20 parallel rows (Fig. lc). The joint between peg and cuticle is set at an angle so that the pegs point distally, and the base of the peg is surrounded by an asymmetrical socket. There are significant differences in thickness of the peg base, both between C. punctafa and C. dentipes and between the two sexes of each (Fig. 1, Table 1). The distance between neighbouring pegs in a row is 25535pm in the male. The rows themselves are closer together proximally than distally; their mean separation is given in Table 1. These fields of pegs on the fore femora of the males act as a file (pars stridens) during stridulation. In some cases the pegs were found to be worn down in a way that would correspond to this use of the structure (Fig. lc). The limited extent of the worn area indicates that a certain part of the field is used preferentially for stridulation or is particularly exposed to friction. Like other corixids. Corha has a projecting maxillary plate that forms a sharp ridge on the side of the head below the antenna. Its dimensions are similar
in both species and sexes, with height ca. 35 kern and length ca. 100 pm. As Jansson (1972) found in Cenocori.xu, this ridge serves as a scraper (plectrum), against which the file rubs during stridulation. In the typical resting posture, corixids hold on to the substrate only with the middle legs; the swimming legs are stretched out to the sides. Starting from this position-or in a few cases while swimming-the males begin to stridulate by moving the forelegs forward and down so that they pass diagonally over the side of the head. The sound signals are produced when, in the course of this movement, the file is rubbed across the scraper, “against the grain” of the pegs. This kind of sound production appears to be typical of the Corixinae (Jansson 1972). We shall describe the stridulatory sounds first as the stridulation movements differ in some of the various songs. The stridulatory sounds Here the term “stridulatory sound” refers only to the sounds produced by the typical stridulation movement of the forelegs. Other sounds made by the animals-for example. during cleaning, diving and copulation-are not treated here. In accordance with the nomenclature suggested by Broughton (1963) and adopted by Jansson (1973) for corixid songs, the song repertoire of various species consists of one or more songs, each of which can consist of one or more verses (Fig. 2). The songs are composed of several distinct pulse trains (Fig. 2d,e). The individual pulses in a train are resolved in Fig. 2e; the time course of the single pulse has been described elsewhere (TheiD 1982). We shall refer to the mean of the peak amplitudes of the pulses within a pulse train as the pulsetrain amplitude. The song repertoire
of C. dentipes
A population of male C. dentipes routinely produces four clearly distinguishable songs. Because their biological significance is not yet clear, they will be designated here by the letters A, B, C and D. Isolated individual animals are capable of singing all four songs. The most important data are summarized in Table 2. Song A (Fig. 2a). The song begins relatively faintly, with alternately higher and lower pulse-train amplitudes. This initially alternating rhythm usually persists only for the first quarter of the song, after which it gives way to an irregular sequence of loud pulse trains with a few faint trains interspersed. On the whole the intensity of the sound increases up to the middle of the song and then decreases toward its end (Fig. 2h). The pulse-train repetitionrate is roughly constant over Table 1. Diameter of peg base and distance between peg rows in C. dentipes and C. punctnru. in the middle of the file. Means +SD for 20 individual measurements of at least 5 anjmals Peg diameter (m) C. denripes ,J C. punctata J C. dentipes i c. punl’mtcr +
13.1 kO.1 7.7 f 0.8 8.2 k 1.0 3.8 f 0.3
Row distance (mrm) 51.5 40.0 38.0 20.7
+ 3.6 t4.6 k 3.2 & 4.0
Fig. I. Thickened bristles (pegs) in a C. punctatumale (d) and female right foreleg. The arrows in (c) are are worn down more than others. fronto-lateral
the middle of the file of a C. dentipes male (a) and female (b) and (e); (c) entire file of a C. puncrutamale. cx coxa, fm femur of the aligned with a row of pegs; note that some of the pegs in the file f-h scraper (arrows) on the right side of the body, as seen from (f), ventro-lateral (g) and along its ridge (h).
763
Sound
production
the entire duration of the song. The ratio of pulse-train duration to the duration of the pauses between consecutive pulse trains is about 1 : 1. Sometimes additional brief low-amplitude pulse trains (l-3 pulses) appear within the pauses (arrows, Fig. 2a). Song B. With only a few exceptions, the song consists of a sequence of several similar verses separated by brief pauses. This song is usually followed immediately by Song C (B + C, Fig. 2h). A verse of Song B typically has a fairly faint beginning and a louder pauses
ending (Fig. 2b). During the initial part the between the pulse trains can become very brief
or be entirely eliminated. Often an isolated pulse train near the beginning is exceptionally loud (arrows, Fig. 2b). During the louder final part, the number of pulses per train is distinctly lower than in the initial part or in Song A. In the extreme case only 1 pulse per “train” is produced. Accordingly, the pauses between the pulse trains are longer than in the initial part. The pulse-train rate of a verse of Song B is significantly higher than that in Song A. When several verses of
7Gmx
h
-
by Corixids
165
Song B are sung in succession, the pulse-train rate and the intensity rise progressively. Song C. Normally C is sung as a continuation of Song B. Although the two songs closely resemble one another in structure, they are presented separately here because one is frequently sung without the other. The initial part of C corresponds to a continuation of Song B except that there are no pauses between the verses (Fig. 2h). Pulse-train rate and intensity continue to increase in each successive verse until Cm,, (Fig. 2~). In the subsequent final part, verse C,,d, the song dies away. The pulse-train rate of Ce,d corresponds to that of Song A, being only half as high as in C max. The repetition rate of the pulses within a train is correspondingly lowered (Fig. 2e). Song D. This song is sung less commonly than the others (TheiD in preparation). In structure it resembles Song B + C (Fig. 2h), in that D too is composed of a sequence of similar verses at progressively increasing intensity and gradually dies away in the final part. But the pulse-train pattern of the individual verses is
--Cend
10s
n
Fig. 2 a-f. Oscillograms of the stridulatory sounds of C. dentipes males: a initial part of Song A; b two verses of Song B; c two verses of Song C and initial part of verse Cend; d transition from C,,, to Cend (section taken from c); e last pulse train of C,, and first pulse tram of C,, (section taken from c): f two verses of Song D. g Two verses of the song of C. punctata males. h Typical time course of complete songs after rectification and integration for recording on a pen-writer. Arrows: see explanations in text. For analogy with other songs, Song B is defined somewhat differently here than by TheiD (1981).
166
JOACHIM THEISS et al. Table 2. Quantitative description of the songs of male C. dentipes and C. punctata. 1st column: means + SD of 10 complete songs in each case. 2nd and 3rd columns:
except for Song A the data refer to the middle part of the verses, in the case of Song C to Cmax: n = 20. Water temperature 12-l 5°C
Duration of the song (s)
Number of pulses per pulse train
B c
21.9 + 4.0 77.0 t 9.3 66.7 f 6.9
10.8 +_2.5 11.7 f 1.0 11.4 + 1.4
D C. punctata
84.7 ? 11.5
11.9 +0.7
47.5 k 7.0
10.8 + 1.0
Pulse-train rate (pt/s)
C. den tipes A
much less regular than in Songs B and C. It is typical of the individual verses in D that 34 pulse trains are especially emphasized (arrows, Fig. 2f). Moreover, the song is fainter than B $ C. The song of C. punctata
Although the stridulatory sounds of this species were monitored regularly over a 2-year period, only one type of song was recorded. It differs from songs of male C. dentipes; of the four, it resembles Song D most closely, but it is significantly shorter (Fig. 2; Table 2) and on the whole fainter. As in Song D of C. dentipes, occasional pulse trains within a verse are emphasized (Fig. 2g). When the stridulatory sounds of the two species are compared, it is striking that C. puncfata males produce considerably less predictible sound patterns. Often no specific pattern is detectable, and the song cannot be subdivided into a sequence of similar verses. Soundproducing
4.3 * 0.4 6.7 + 1.0 8.6 + 1.0 Gl,,) 4.7 f 0.3 4.8 +0.3
C. dentipes males the mean distance between the 11 rows of pegs in the middle of the file area is about 46 pm. Therefore when the direction of motion is such that the scraper moves almost perpendicular to the peg rows the mean repetition rate of the pulses in a train would be ca. 150 pulses/s. It can readily be calculated from the data in Table 1 and Fig. 5 that the measured pulse rate in a train averages ca. 140 pulses/s, which is approximately consistent with the prediction. Each sound pulse corresponds to one row
mechanism
To reveal in greater detail the relation between leg movement and sound pattern, C. dentipes males were filmed while producing Song A and the stridulatory sounds were synchronously tape-recorded. Singleframe analysis gave the following results. In the examples of Figs 3 and 4, the left leg is moved up and down at about twice the rate of the right leg, with no clear phase relation between the two (Fig. 4). The downstroke of the leg is slower than the upstroke. Only during the downward movement of the left leg is a pulse train produced (Fig. 3). The phase relation between the movement of the left leg and the production of a sound is within the resolution permitted by the frame rate (Fig. 4). It was also evident in the film that the right leg is not held as close to the head as the left leg. In a given individual the right Ieg can have the more rapid rhythm during some renditions of Song A and the left leg during others. The same movements are also observed at lower water temperatures. It is very likely, therefore, that Song A is produced with only one leg. At each movement of the file over the scraper a pulse train is produced; thus the pulse-train rate of Song A corresponds to the rhythm of the more rapidly moving leg. The velocity v with which the file moves over the scraper can be estimated from the films. During the performance of Song A at 2O”C, v is ca. 7mm/s. In
Fig. 3. Movements of the right (0) and left (0) forelegs of two C. dentipes males during two phases of Song A (a initial segment, b middle segment). Above each graph is an oscillogram of the synchronous record of the sound. At the bottom is a scale showing the timing of the consecutive frames of the films (96 frames/s), with drawings of every third frame for (b). Ordinate: distance of the femur-tibia joint, in the plane of the picture, from an intermediate position ( = 0). Water temperature 20°C.
161
Sound production by Corixids
.
or, a b
06
1
05-l
1
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.
.
**
.
.
.A
AA
.
.
1 . *....
.
.
.
.
.
-
.t
.
.
.
.
.
.
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.
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7
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c
d
Fig. 4. a Time difference between the highest point of the leg movement (right A., left 0) and the middle of the next pulse train, for a section of Song A of a C. dent&es male. b Up-and-down movement of the right leg and c of the left leg. d. Oscillogram of the song. Data obtained from films as in Fig. 3.
of pegs moving across the scraper. Comparison of the size of the scraper and the distance between the pegs (Fig. 1) shows that the scraper encounters at most 3 adjacent pegs in a row on each passage. Observation of the stridulation movements at low water temperature was sufficient for describing the movements in the following songs. Unlike Song A, Song B is produced by alternating movements of the two legs, a pulse train being produced by each downstroke. During the louder terminal part of each individual verse the fore femora are held at a steeper angle. The same is true of Song C up to the verse C max. In the subsequent verse C,,,. as the song fades away, the pulse trains are produced by only one leg; the other is hardly moved. Because the soundproducing leg continues in the same rhythm as during Cma: the pulse-train rate is halved. Surprisingly, the pulse repetition rate within each train is also reduced (Fig. 2d,e). This finding indicates that during this verse the downstroke of the sound producing leg is slower than during C,,. As in Song B, the first part of each verse of Song D is produced by alternating movements of the two legs. In the middle of the verse the rhythm changes ; one leg is held at a steeper angle and the other stops stroking briefly. The final part of D, like Cen& is performed with only one leg. The sequence of. leg movements in stridulating C. punctuta males is like that in Song D of C. dent&s males but considerably more variable. Influence of temperature on the stridulation movements
Both the repetition rate of the sequence of leg movements and the velocity of each movement depend on temperature. As a result, the pulse-train rate and the pulse rate within a train depend on the temperature
of the water. The influence of the water temperature on the pulse-train rate was examined quantitatively for Songs A and C of C. &wipes males between 4 and 25°C. Qn a semilogarithmic plot (Fig. 5) the data depart slightly but distinctly from a straight line, indicating that in the range of temperatures studied Qio is not constant. For Song A the QiO in the range 414°C is 2.7, whereas in the range 15-25°C the QiO is 2.0. At temperatures above 20°C only Song A is performed. The pulse-train rate of C,, is always twice that of Song A and of Cend, regardless of the temperature. Taking into account that the precision of the temperature measurements is no greater than a 1°C the scatter of the data is very slight; the standard deviation for Song A and Cend is + 0.3 pt/s, independent of + 0.2 pt/s and for C,,,, temperature. The influence of the temperature on the duration of stridulation varies among the different songs (Table 3). Song A is shortened much more at higher temperatures than is the song combination B + C. This effect is only partially due to the fact that at higher temperatures a larger number of B verses are sung before the transition to C. Whereas the total number of pulse trains in Song A-and thus the number of downstrokes of the stridulating leg-is about the same at 5°C as at 20°C the number of pulse trains in Song B + C is about doubled. There is no significant influence of temperature on the ratio of pulsetrain duration to pause duration. The pulse rate within a train exhibits the same temperature dependence as the pulse-train rate. Soundpressure level (SPL) of the stridulatory sounds The SPL values for the largest pulse per train, averaged over complete songs (SPL,) of males of three corixid species, are shown in Table 4 together with the largest measured single values. The SPL, for the verse C maxof C. dentipes is about 10 dB higher than that for Song A. The singing of C. dentipes, then is
1
0
5
0
15
20
oc
, 25
Lo
Fig. 5. Pulse-train rates (log scale, left ordinate) of Song A (0) verse C,, (D) and C,,,(A) as a function of water temperature. Means of 20 individual measurements of long sections of the songs of 5 C. dentipes males. For comparison, data of Song A (0) &SD with a linear scale (right ordinate.)
768
JOACHIM
THEISS
et
al.
Table 3. Temperature dependence of the songs A and B + C of C. denfipes males, for the water temperatures 5 and 20°C. T. mean overall song duration at 5 ‘C (T,) and 2O~C (T,), for 20 songs in each case; pulse-train rate of Song A from Fig. 5 5C Song A Duration Pulse-train Pulse rate
rate
Song B -1 C Duration Pulse-train rate Number of verses
about
T, - 74 t 10.6 s 1.8ptjs 40 p/s T, - 190 k45.7 2.9 pt/s 9.0 + 2.9
10-20 dB louder than that of C. punctata
Callicarixa
20 c
and
praeusta.
Because of the marked fluctuation in intensity of the pulse trains, especially in Song A (Fig. 2a). the percentage distribution of the highest SPL in the measured pulse trains is shown as a histogram with 5-dB class width in Fig. 6. The distribution has a maximum that coincides roughly with the mean SPL,. About 90% of the values are above 100 dB re 1 @a. When one animal in a population of C. dentipes males begins to sing Song A, often one to several conspecifics join in the song (choral stridulation). The SPL, of such choral stridulation is higher by 3.5 dB than that found for individual animals (Table 4). Accordingly, relatively high pulses occur more frequently during choral stridulation than during individual songs (Fig. 6). This observation can be explained by summation of single pulses produced by different animals (c.f. also Finke and Prager 1980). It remains to be learned whether individual animals also intensity during choral increase their sound stridulation. For one typical Song A the SPL of each pulse was measured. Fig. 7a shows the distribution of pulse amplitudes in the song. They are not normally distributed, because the song begins with a fainter section and also dies out gradually. Within a pulse train, the pulses near the middle have higher amplitude on the average (Fig. 7b).
Comparative
aspects
4.5
T, = 16 f 2.2 s 7.1 pt/s 140 p/s s
T, = 114 k34.8 10.7 pt/s 14.5 f 5.0
s
1.7
Table 4. Peak SPL of the largest amplitude pulse in each pulse train, averaged over 10 complete songs in each case + SD (SPL,). and the largest single value obtained (SPL,,,), in dB re 1 pa. Distance from animal 0.1 m. In choral stridulation 2-4 animals sing simultaneously SPL, C. dentipes (Sow A) Single Chorus c. punctntu Call. praeusta
115.0 118.5 105.4 107.2
SPL,,,
k4.4 +2.7 f 4.4 * 3.3
133dB 119dB 117dB
With regard to the temporal structure of the songs, only Song B + C differs distinctly from all the other songs; the pulse-train rate is significantly higher and rises during the song, while the number of pulses per pulse train becomes smaller at the end of each verse. The differences among the Songs A and D and the song of C. puncrata lie in their duration and intensity modulation. According to Jansson (1973), stridulatory
30 % 26
DISCUSSION
T,/T,
1
22
al‘ carixid sound signals
There are distinct differences between the sounds produced by male C. dentipes and C. punctata. The most conspicuous of these are (1) the extensive repertoire of C. dentipes as compared with the single song of C. punctata, (2) the greater precision in the stridulatory pattern of C. dentipes as compared with the variability, even within an individual, of the sound patterns of C. punctata, and (3) the lo- to 20-dB higher intensity of the C. dentipes songs. It can be concluded from these differences that a species-specific sound pattern is far more significant for C. dentipes than for C. punctata. This conclusion is supported by the observation that the stridulation and reproductive phase of C. punctata begins some months prior to that of the competing C. akntipes (TheiB 1981).
6
106
113
118
123
1
Fig. 6. Distribution (in 5-dB classes) of the peak SPLs of the largest pulse per pulse train in 10 complete examples of Song A from various individual animals (shaded columns) and in 10 choral songs (white columns; 24 C. dentipes males singing simultaneously); dB re 1 @a, 0.1 m from animals to hydrophone.
Sound
production
769
by Corixids
1
111 b dB
107
1
20-
!
16-
103-
i
12-
0-
9496
99. 103
N)4106
109. 118 114- ;$-dB 113
95-i,, 12
I
4
I
,
6
,
I
8
I,
10
I
I,
12
N
I 14
Fig. 7a.b. Peak SPL of all the pulses in a typical Song A that exceed 89 dB re 1 pa (0.1 m from animals to hydrophone). a Distribution of the peak SPL of all the 732 pulses in the song, in 5-dB classes. b Peak SPL of the Nth pulse in a pulse train, averaged over all the 79 pulse trains in the song &SE (standard error). The numbering of the pulses was centered on the middle of the pulse train, the number N = 7 being assigned to the middle pulse in each case. Because the number of pulses per train varied between 3 and 14, the means were calculated from varying numbers of single values (n) (smallest n = 28); pulses numbered 1,2 and 14 were so rare that no mean was calculated.
sounds of the genus Cenocorixa serve as a premating isolation mechanism. In this genus, pulse rate and pulse-train rate evidently play a subordinate role in specificity, for there is extensive overlap of these features among the various species (Jansson 1974). In the Orthoptera the syllabic pattern of the songs (a syllable is equivalent to a pulse train), and in some cases the amplitude modulation of the single syllable, is crucial for recognition of the conspecific signal (review by Elsner and Popov 1978 ; von Helversen 1979; Weber et al., 1981; Thorson et al., 1982; cf. also Gogala 1970 for Cydnidae). Schulze (1977) described only one type of song produced by male C. dentipes. His published data on the structure of the song indicate that it was the one here called Song A. He could not observe the other songs because in his experiments the water was kept at a constant temperature of 22°C; our own observations show that at temperatures above 20°C only Song A is sung. As in other corixids (Finke 1968; Jansson 1974), the pulse-train rate of C. dentipes song rises with increasing water temperature. Because the Qio becomes smaller at higher temperatures, this relation cannot be described by an exponential function. Such a decrease of the QiO with rising temperature corresponds to the Arrhenius equation of thermodynamics, and appears to be demonstrable for all movement sequences of poikilothermic animals as long as the range of temperatures tested is not too small. Walker (1975) has proposed a linear model to describe the temperature dependence of movement cycles of poikilothermic animals, and has documented such linearity for the wing-beat rate of stridulating orthopterans. Over the entire 21°C temperature range studied, the temperature dependence of the pulse-train rate of C. dentipes departs distinctly from linearity (Fig. 5). This is also the case for some species of Cenocorixa (Jansson 1974). Comparison of the correlation coefficients of the linear and exponential regression curves as done by Walker (1975) does not seem to us to be appropriate here,
measured here obviously lie between an exponential and a linear function (see Fig. 5). Data on the sound pressure levels (dB re 1 pa) generated by stridulating corixids are available for several species : Sigara striata (122-125 dB at a distance of 0.12-O. 15 m from the animal) and Callicorixa praeusta (102-108 dB, Finke 1968) Corixa dentipes (101-l 11 dB, Schulze 1977), and Palmacorixa nana (11 l-124 dB, Aiken 1982; 100 dB must be added to the values 1l-24 in Aiken 1982 (Aiken personal communication)). All these measurements were done in small containers, and in no case is it stated whether the peak SPL of single pulses is meant. According to our observations, S. striata stridulates about as loudly as C. dentipes. Therefore Finke’s data probably refer to the peak SPL actually produced. Sound-intensity measurements we did as a control on Callicorixa praeusta (Table 4) confirm Finke’s results. Schulze estimated the loudness of the C. dentipes songs by the fact that the stridulation was just barely audible outside the aquarium. His estimate is about 1&20dB lower than the values we measured. The dynamic range of 18.5 dB given by him is incomprehensible; with an A-weighted background noise < 70 dB in our measurements, the range of pulse amplitudes produced by C. dentipes amounts to ca. 60 dB (Table 4). since the data
Estimation of the sound pressure level at the tympanal organs
Sound radiation in corixids is brought about by volume pulsations of the respiratory air bubble of the physical gill, and a spherical air bubble can be used to first approximation as a model of this emitter (Then3 1982). For an air bubble oscillating underwater at its natural frequency such as to generate an SPL of 131 dB re 1 $a at a distance of 0.1 m, it can be calculated that the radius changes by Ai = 0.8 m (Eq. (l), Appendix). It follows that the maximal oscillation amplitudes of the air-bubble surface of a stridulating animal can be estimated at a few nrn.
770
J~ACHIM THEISS et al.
The threshold curves of the thoracic tympanal organs, in contact with air even in submerged corixids, have been measured with airborne sound for C. punctata (Prager 1976; Prager and TheiB 1982). Until now, alternating pressures which occur within the air bubble of submerged corixids during acoustic communication have been unknown. It therefore appeared particularly interesting to estimate the alternating pressures in the air bubbles of a stridulating animal and in that of a listening animal some distance away, by means of the air-bubble model (see Appendix). The calculations indicate that the pressure within the air bubble of a stridulating animal is ca. 36 dB above the SPL measured 0.1 m away. For a stridulating C. punctata male, then, even the low-intensity stridulatory pulses would be above the threshold of those sense cells in the thoracic scolopale organs that have so far been studied. On the assumption that the average resonance step-up of the sound pressure entering the air bubble of a listening animal is ca. 1OdB (Prager and Streng 1982, TheiB 1982), the mean SPL for the largest pulse in each pulse train of the C. punctata song would be 115 dB within the bubble of a listening animal at a distance of 0.1 m from the singer (Table 4). This means that even at this short distance the entire pulse pattern of the song-including the low-amplitude pulses ,in the train-can be transmitted only by the more sensitive sense cell (Al) in the mesothoracic tympanal organ. If the distance between a singing and a listening animal is still shorter the two animals must be considered as coupled oscillators (c.f. Meyer and Skudrzyk 1953). Soundproducing mechanism The SEM pictures of the file reveal
distinct sexspecific and species-specific differences in the thickness of the stridulatory pegs. In the males the thickness of the pegs is positively correlated with the intensity of the stridulatory sounds. Jansson (1972) found a similar relation in Cenocorixa. Because the stridulatory pegs of C. punctata males are equal in thickness to those of C. dentipes females, one might suspect that in C. dentipes the females are also capable of stridulation. As films and direct observations of stridulation movements indicate, the two forelegs do not simultaneously produce sound in any of the songs of C. dentipes and C. punctata. The contradictory statement by Schulze (1977) should be considered with caution because his observations were made at room temperature with the unaided eye. Although, synchronous downward movements of the forelegs can occur (Fig. 3a), the present results corroborate Jansson’s (1979b) view that in the Corixinae the two legs do not actually produce sound simultaneously. In exceptional cases, when the legs are alternating, the end of one pulse train can overlap the beginning of the next in some songs. Unlike the songs of acridid grasshoppers (Elsner and Popov 1978), the sound patterns of the Corixinae, thus usually consist of distinct pulses and pulse trains, produced by a single leg. The conclusions about the sound-producing mechanism to be drawn from these results are as follows. From the direction of foreleg movement during stridulation and from the structure of the stridulatory apparatus it must be concluded that the pegs in the file with their thickened bases touch only the scraper;
that is, it is not a matter of an entire row of pegs sweeping in a broad front over the side of the head, as in the descriptions of Finke (1968) and Schulze (1977). From the dimensions of the scraper and from the size and separation of the pegs it follows that 1 to 3 adjacent pegs per row catch on the scraper. Because the pegs are seated in the cuticle in such a way that during the downstroke they are inclined toward the approaching maxillary plate, they are especially likely to hook over its sharp edge. The forward movement of the femur drags the head along until the scraper slips off the row of pegs (c.f. Aiken 1982), allowing the head to swing back into its starting position or until the scraper catches in the next row. When it is suddenly released the head, which covers a large area of the animal’s air bubble like a cap, thereby transmits an impulse to the air bubble that sets off volume pulsations of the bubble at its natural frequency. In this way a sound pulse is produced. The weaker pegs in the file of C. punctata displace the head less before it slips off, so that the restoring force is less and the stridulatory signals are not as loud. This explanation of the mechanism of stridulation is supported in principle by studies of the frequency spectrum of the stridulatory pulses and the way the oscillations are damped (TheiD 1982). Acknowledgements: We thank Professor Dr D. Burkhardt and Dr I. Veit for critically reading the manuscript, Miss Helga Vi5lkl for technical assistance and the Deutsche Forschungsgemeinschaft for financial support (SFB 4, Regensburg). APPENDIX I. Let us assume a spherical air bubble under water with volume V, at rest exhibits volume pulsations V, at its natural frkquency o,, (V, = V, + A 3; sin w,, I; A P, 4 V,; cf. TheiD 1982). How large is the radius change Ai, of the pulsating air blbble, if it-produces a sound pressure pl at distance I from the centre of the bubble (2 means peak value of x)? According to Strasberg (1956) the radius change is given by A;,
=
!!!L
3KP where an adiabatic exponent H = I .41 and p = 1atm can be assumed (TheiS 1982). With a peak SPL of 131 dB re 1 PPa at distance I = 0.1 m one obtains A;, = 0.8 pm. 2. How high is the alternating pressure pulsating air bubble in the above case? According to Poisson’s law
pL within
the
By applying Eq. (1) one obtains 6,/b, = (A P,/Ai,) (1/3 Vol. With Ap,/Ai,-df,/d?, it follows that j$/jj, z l/rO. Given an air bubble with a natural frequency f0 = 2 kHz and hence a radius rO= 1.65mm (c.f. TheiD 1982) one obtains pi/p, u 60. Thus, in this example the alternating pressure with the pulsating air bubble has a 36 dB higher level than the SPL measured at a distance of 0.1 m from the centre of the bubble. REFERENCES Aiken R. B. (1982) Sound production and mating in a waterboatman, Palmacorixa nana (Heteroptera: Corixidae). Anim. Behav. 30, 5461.
771
Sound productic )n by Corixids Broughton W. B. (1963) Method in bioacoustic terminolonv. In Acoustic Behaviour of Animals (Ed. by Busnel RYG.), pp. 3-24, Elsevier, Amsterdam. Elsner N. and Popov A. (1978) Neuroethology of acoustic communication. Adu. Insect Physiol. 13,229-3X Finke C. (1968) LautluBerungen und Verhalten von Sigara striata und Callicorixa praeusta (Corixidae Leach : Hydrocorisae Latr.) 2. Vergl. Physiol. 58,398422. Finke C. and Prager J. (1980) Pulse-train synchronous pair-stridulation by male Sigaru striata (Heteroptera: Corixidae). Experientia 36, 1172-l 173. Gogala M. (1970) Artspezifitlt der LautluBerungen bei Erdwanzen (Heteroptera: Cydnidae). 2. Vergf. Physiol. 70,20-28.
Helversen 0. von (1979) Innate recognition of acoustical patterns and its significance for the isolation of species. Verb. dt Zool. Ges., Gustav Fischer Verlag, Stuttgart, p. 42-59. Jansson A. (1972) Mechanisms of sound production and morphology of the stridulatory apparatus in the genus Cenocorixa (Hemiptera: Corixidae). Ann. Zool. Fennici 9, 120-129. Jansson A. (1973) Stridulation and its significance in the genus Cenocorixa (Hemiptera: Corixidae). Behaviour 46, l-36.
Jansson A. (1974) Effects of temperature on stridulatory signals of Cenocorixa (Hemiptera: Corixidae). Ann. Zool. Fennici II,2888296.
Jansson A. (1976)Audiospectrographic analysis of stridulatory signals of some North American Corixidae (Hemiptera). Ann. Zool. Fennici l&4862. Jansson A. (1979a) Reproductive isolation and experimental hybridization between Arctocortsa carinata and A. germari (Heteroptera: Corixidae). Ann. Zoo/. Fennici 16,89-104.
Jansson A. (1979b) Experimental hydridization of Sigara srriata and S. dorsalis (Heteroptera: Corixidae). Ann. Zool. Fennici 16, 105-l 14. Meyer E. and Skudrzyk E. (1953) Uber die akustischen Eigenschaften von Gasblasenschleiem in Wasser. Acustica 3.434440.
Prager J. (1976) Das mesothorakale Tympanalorgan von Corixa punctata Ill. (Heteroptera: Corixidae). J. Comp. Physiot. 110, 33350.
Prager J. and Larsen 0. N. (I 98 1) Asymmetrical hearing in the water bug Corixa punctata observed with laser vibrometry. Naturwissenschaften 68, 5799580. Prager J. and Streng R. (1982) The resonance properties of the physical gill of Corixa punctata and their significance in sound reception. J. Comp. Physiol. 148,323-335. Prager J. and TheiD J. (1982) The effect of tympanal position on the sound-sensitivity of the metathoracic scolopale organ of Corixa. J. Insect Physiol. 28, 447452.
Schulze M. (1977) Biophysik der Unterwasserlauterzeugung am Beispiel der Ruderwanze Corixa dentipes Thms. Zool. Beitr. 23,477-507.
Stichel W. (1935) Illustrierte Bestimmungstabellen der deutschen Wanzen. Selbstver., Berlin. Strasberg M. (1956) Gas bubbles as sources of sound in liquids. J. acoust. Sot. Am. 28,20-26. TheiD J. (1981) Schallerzeugung und Stridulationsaktivitat bei Corixiden. Mitt. dt. Ges. ANg. Angew. Ent. 3, 235238.
TheiO J. (1982) Generation and radiation of sound by stridulating water insects as exemplified by the corixids. Behav. Ecol. Sociobiol.
10, 225-235.
Thorson J., Weber T. and Huber F. (1982) Auditory behavior of the cricket. II. Simplicity of calling-song recognition in Gryilus, and anomalous phonotaxis at abnormal carrier frequencies. J. Comp. Physiol. 146, 361-378.
Walker T. J. (1975) Effects of temperature on rates in poikilotherm nervous systems: evidence from the calling songs of meadow Katydids (Orthoptera : Tettigoniidae: Orchehmum) and reanalysis of published data. J. Comp. Physiol. 101,5749.
Weber T., Thorson J. and Huber F. (1981) Auditory behavior of the cricket. I. Dynamics of compensated walking and discrimination paradigms on the Kramer treadmill. J. Comp. Physiol. 141, 215-232.