Journal J. Comp. Physiol. 135, 259-268 (1980) of Comparative Physiology, A by Springer-Verlag 1980

Insect Disturbance Stridulation: Characterization of Airborne and Vibrational Components of the Sound

W. Mitchell Masters* Section of Neurobiology and Behavior, Cornell University, Ithaca, New York 14853, USA

Accepted October 18, 1979

Summary. Some stridulate when attacked by 1 kHz. The average decrease in power above this fre- a predator. This behavior has been interpreted as quency is about 12 dB/octave. The maximum peak-to- a defensive response, the sound being a warning to peak amplitude of cuticular motion is about 1 to predators of the 's noxiousness. Since to humans 10 gm. many such disturbance sounds are audibly similar, These common characteristics may lead predators it is possible that they may in fact be mutually mi- to treat insects producing disturbance sounds simi- metic. This idea was investigated through analysis larly, although this possibility should be tested empiri- of the temporal and spectral characteristics of the cally. If acoustic mimicry exists, the communicatory disturbance sounds of a variety of insects that stridu- interchange between predator and prey may be subtler late by a file-and-scraper device. Properties of both than is commonly appreciated. the airborne sound and the underlying cuticular vibra- tion (detected by a special vibration measuring instru- ment) were examined, and four characteristic features found: Introduction 1. The temporal pattern is simple. Bursts of tooth- strike impulses are about 80 ms long, and are sepa- When insects are handled or restrained, some respond rated by pauses about 90 ms long. Bursts occur at by emitting sounds, variously known as disturbance, a rate of about 5 to 10/s. distress, alarm or warning cries. Alexander (1967), 2. The temporal pattern is irregular. For tooth- in his classification of insect acoustic signals, reported strike interval, burst duration, pause duration and that more examples fell into the category of distur- interburst interval, the standard deviation is usually bance sounds than into any other. Yet, despite the > 30% of the mean. Much of the irregularity is pre- great number of disturbance sounds known, their sumably caused by the insect struggling at the same function has not been well established. They have time it stridulates. Some insects show less variability, been thought to aid insects when they are attacked and these appear to lack tight coupling between stri- by predators (see Haskell, 1961), either because the dulatory movements and struggling movements, so sound startles the attacker and causes it to hesitate struggling does not interfere with stridulation. momentarily, thus increasing the chance of the in- 3. The airborne sound pressure waveform is im- sect's escape, or because the sound is a warning, in pulsive. The frequency coverage of the sounds is quite the manner of an aposematic visual signal, that the broad with an average 10-dB bandwidth of about insect has an effective and perhaps punishing defense. 40 kHz centered at 25 kHz. The sounds are not in- Only recently have experimental studies shown that tense, ranging from about 10 to 60 dB (re disturbance sounds apparently do deter some preda- 20x 10 .6 Pa) at 10 cm. tors (Bauer, 1976; Sandow and Bailey, 1978; Smith 4. The cuticular vibration waveform is sharply and Langley, 1978; Masters, 1979a). peaked and contains maximum energy at a frequency To the human ear, many insect disturbance sounds determined by the tooth-strike rate, usually about are remarkably similar. This raises the interesting pos- sibility that predators also perceive these sounds as * Present address: Fakult/it ffir Biologie, Universit/it Konstanz, being alike, and that disturbance sounds might be Postfach 5560, D-7750 Konstanz, Federal Republic of Germany the functional mode linking a large mimetic assem-

0340-7594/80/0135/0259/$02.00 260 W.M. Masters: Insect Disturbance Stridulation blage. The advantage to members of such an assem- bined frequency response of the microphone-amplifier-tape record- blage, supposing that disturbance sounds are sematic, er combination was approximately +2.5 dB over the range 0.5 would be much the same as for visual mimicry (see to 100 kHz. Sound recordings were made inside a sound attenuating room Edmunds, 1974): members could share the burden at a temperature of 22,+ 2 ~ In order to reduce sound reflections of educating predators, and at the same time simplify inside the room, urethane foam pads (about 2 x 1 x 0.1 m) were the learning task required of predators by standardiz- hung approximately 10 cm from the walls and ceiling. To reduce ing the warning stimulus. However, the idea of acous- reflections at high frequencies still further, wedgeshaped fingers of foam (base 4x2.5 cm, height 10 cm) were glued to the inside tic mimicry requires more rigorous substantiation of a corner cube formed by three sides of a corrugated cardboard than subjective appraisal by the unaided ear. In this box 80 cm on a side. This corner was placed in front of the ring- paper I analyse the physical characteristics, both air- stand mounted microphone at a distance of about 1 m. For sound borne and vibrational, of the disturbance sounds of recording, insects were held in front of the microphone by their a number of insects. The study is restricted to those legs, either by hand or with forceps, at measured distances marked on a 1 mm diameter wire extending out from the microphone. insects that use a file-and-scraper mechanism, proba- Insect surface vibration was measured using a non-contact, bly the most common method of sound production optical technique (Masters, 1979b). The vibration response of the among insects (Dumortier, 1963 a). The results of the instrument was _+ 1.5 dB between 10 Hz and 120 kHz. The signal analysis suggest that, generally, disturbance sounds and calibration outputs of the vibration detector were recorded on the two channels of a stereo tape recorder (Uher 4400 Report possess several characteristics in common, which to- Stereo) having a frequency response of _+ 1.5 dB from 20 Hz to gether might identify the sounds. This might lead 18 kHz, down 5.5 dB at 20 kHz. Usually vibration at only one predators to treat the sounds, and the insects that point on the cuticle was measured for each insect. On produce them, similarly. the point was on one wing cover, whereas on mutillids it was in the middle of the second abdominal tergite, to which the scraper is attached. Setae around the point of vibration measurement were scraped off so that they would not interfere with light reflection from the cuticle. In order to record vibrations from those insects Materials and Methods with non-shiny cuticle, it was usually necessary to stick a small (~ 1 mm 2) piece of aluminized mylar (video splicing tape) to the The insects used in this study were collected at the Archbold Biolog- point on the insect which was to be examined. This increased ical Station, 12 km south of Lake Placid, Florida, during the sum- the sensitivity of the technique (Masters, 1979b), and for some mers of 1976 and 1977. One or more species from the families insects it was the only way to obtain an adequate signal-to-noise , Cydnidae, Carabidae, Hydrophylidae, Passalidae, Sca- ratio. Addition of the tape should have had negligible influence rabidae, Cerambycidae and were used, with the majority on the vibration of the cuticle, since the mass of the tape was of the specimens being cerambycids or mutillids. Most insects were small (24 l.tg/mm2) and its stiffness much less than that of the taken at light traps at night, but velvet (Mutillidae) were cuticle. collected during the day as they wandered over sandy, cleared areas. Temporal Analysis. Disturbance sounds produced by insects having The files and scrapers of representative insects were investi- file-and-scraper devices are generally structured as a series of im- gated using a scanning electron microscope (AMR-1000A, Ad- pulses, called tooth strikes, each produced by impact of the scraper vanced Metals Research, Bedford, MA). The specimens were dried against a ridge, or tooth, of the file. A single pass of the scraper by the critical point method (Samdri PVT-3, Tousims Research along the file (or some portion of it) gives rise to a series of Corp., Rockville, MD) and sputter coated with palladium-gold tooth strikes which I call a burst. Between bursts are pauses caused (Samsputter 2A, Tousims Research). In mutillids the file is located when the file stops or reverses its motion, or when the file and ventromedially on the third abdominal tergite. The scraper is on scraper are disengaged. (In some cases the file is pulled across the caudal edge of the second tergite and lies over the central the scraper rather than vice versa, but throughout this paper I portion of the file. The third abdominal segment fits partially will assume that the file is stationary and the scraper is pulled inside the second and during stridulation it is moved in and out across it.) The interval from the beginning of one burst to the of the second segment like a piston in a cylinder. The file of beginning of the next I call the interburst interval and its reciprocal cerambycids is located ventromedially on the anterior portion of the burst rate. the mesothorax just forward of the points of attachment of the For temporal analysis of disturbance sounds, the tooth-strike elytra. The scraper is found on the caudal edge of the prothorax rate, burst duration, pause duration and interburst interval were and lies over the file. During stridulation the prothorax is bent measured from recordings of the airborne sound. Tooth-strike rate alternately downward and upward so that the scraper moves back was determined on a computer (Digital Equipment Corp. Lab 8/E) and forth over the file. using an interval histogram program supplied by the manufacturer. Histograms covered a time range of 4.8 ms in 24 divisions (bins), Recording Sound and Vibration. Airborne sounds were recorded with a 25th or overflow bin counting the number of tooth-strike with a Granath-type ultrasonic microphone (McCue and Bertollini, intervals longer than 4.8 ms. For a few insects with a slow tooth- 1964), calibrated in free-field relative to a Bruel and Kjaer model strike rate (long tooth-strike intervals), the time range was increased 4135 6-mm microphone using the frequency response information to 9.8 ms in 49 bins plus a 50th overflow bin. Counts in the overflow provided by the manufacturer ('_+ 1 dB, 4 Hz-100 kHz). The re- bin were not included in statistical computations. sponse of the Granath microphone was _+4 dB from 0.5-100 kHz. Analysis of burst duration, pause duration and interburst inter- This was improved to _+ 1.5 dB over the same range by an electronic val was done by filming the filtered (> 3,000 Hz) airborne distur- equalization network. Sounds were recorded at 76 cm/s on an in- bance sounds at 20 mm/s on a kymograph camera (Grass Instru- strumentation tape recorder (Lockheed model 417), the frequency ments model C4N), producing traces similar to those shown in response of which was _+ 2 dB between 0.5 and 100 kHz. The corn- Fig. 3. Bursts and pauses were then measured to the nearest 0.5 mm W.M. Masters: Insect Disturbance Stridulation 261

(12.5 ms) and entered sequentially into a computer data file for determined by averaging 30 noise spectra in tl~e same manner. analysis. A specially written program compiled histographic and The final averaged spectrum for each insect was obtained by sub- statistical data on burst duration, pause duration and interburst tracting, rms-fashion, the average noise power at each frequency interval (calculated by adding successive burst-pause pairs). The from the average signal-plus-noise power. (A signal-plus-noise program accumulated counts in 40 bins, each 12.5 ms wide, over reading 3 dB above the average noise level is therefore reduced a period of 0.5 s. Times longer than 0.5 s were accumulated in by 3 dB, while a reading 10 dB above noise level is reduced by an overflow bin and were not included in the statistical analysis. 0.5 dB).

Spectral Analysis. Spectral (frequency) analysis of sound and vibra- Statistics. Means were compared (P<0.05) by two-tailed t-tests tion was done using a Fast Fourier Transform (FFT) computing for unequal sample sizes and unequal variances (Guenther, 1973). spectrum analyzer (Nicolet Mini-Ubiqnitous 444A). This instru- The skewness of distributions was determined (P< 0.02) by a two- ment digitized 1,000 points in a time segment of the signal, the tailed test of skewness (Snedecor and Cochran, 1967). The coeffi- length of which depends on the analysis range setting (4 ms on cient of variation C (standard deviation divided by the mean, the 100 kHz range and 20 ms on the 20 kHz range). It then com- Snedecor and Cochran [1967]) was used to assay the relative varia- putes a 400 point discrete Fourier transform of the digitized signal tion of different distributions. There is no agreed upon value of using the FFT algorithm. The result is plotted as a power spectrum C that signifies whether or not a particular distribution shows (power versus frequency). high variability. In this paper, C>0.30 (standard deviation > 30% Airborne sound spectra were averaged because disturbance of mean) is taken to mean a set of measurements shows large sounds, even for one insect, were variable in frequency composi- variability or irregularity. C< 0.20 shows little variability. By way tion. Furthermore, it was often difficult to distinguish signal from of supporting the reasonableness of these limits, for calling background noise, both because disturbance sounds are rather songs, which are usually thought of as rather regular, most (al- noiselike in character and because the signal-to-noise ratio for though not all) temporal parameters show little variation (C< 0.20, many of the softer sounds was very low. Consequently, averaging calculated from data in Bentley and Hoy [1972]). gave a better idea of the spectral characteristics of each insect's sound and of the background noise level. Averaging was done Results by measuring the rms level at 40 different frequencies on each spectrum using a digitizing tablet (Intelligent Digitizer, Sum- magraphics Corp., Fairfield, CT) and then computing the mean The files of a mutillid wasp ( lepeletierii) and standard deviation at each frequency. Eight disturbance sound and of a cerambycid ( rufulus, in- spectra were averaged for each insect. The background noise was sect # 104) are shown in Fig. 1. In both cases, as

Fig. la-d. Scanning electron micrographs of the files of a mutillid wasp Dasymutilla lepeletierii (a and b) and a cerambycid beetle Enaphalodes rufulus (c and d). Upper photographs show the files in close-up and lower photographs show details of the file ridges. Calibration bar on the upper photographs 50 p.m, on the lower photographs 2 gm 262 W.M. Masters: Insect Disturbance Stridulation is typical of insect files, the ridges, or teeth, of the file, which appear as striations in the upper photo- graphs, are spaced at quite uniform intervals. Tooth .oo spacing is ~ 5 gm for the mutillid and ~ 7.5 gm for 400 the cerambycid. Tooth profile, however, is different in the two insects, as shown in the lower two photo- 0 n graphs where a scratch on the file reveals the cross- section of the teeth. The mutillid file is almost rectan- gular in profile with ridges ~ 2 gm wide and ~ 1 ~tm deep, while the cerambycid file shows an undulating surface with a peak-to-trough depth of ~2.5 gm. iiit o o Temporal Pattern Analysis ool_

For each of 42 insects, between 400 and 5,000 (average 2,000) tooth-strike intervals were timed. The average oot/L interval and standard deviation was 1.1 + 0.5 ms. His- r-1 --. 0 tograms of tooth-strike intervals for representative insects are shown in Fig. 2. (Data on individual in- sects are contained in Masters [1979c].) All but one 800 t of the tooth-strike distributions was skewed posi- tively, signifying that they had longer tails on the right than on the left. The coefficient of variation O rl C was high, ranging from 0.28 to 0.76. Variation "'tL in tooth-strike interval is in line with that reported e by Markl et al. (1977) and Markl and H611dobler .oot (1978) for disturbance stridulation, where C calcu- lated from their data ranged from 0.21 to 0.89. 400~ L Oscilloscope traces of the amplitude envelope of representative disturbance sounds for insects from i s 4 5 z 3 4 5 five families are shown in Fig. 3. From records like msec these, the temporal structure of the disturbance Fig. 2a-j. Tooth-strike interval histograms for individual insects. sounds of 35 insects was analysed. Between 24 and a Arilus cristatus # 127 (Reduviidae); b Omophron labiatum ~/115 545 burst/pause pairs (average 110) were measured (Carabidae); c Tropisternus collaris # 118 () ; d Hybo- sorus illigeri #I 117 (Scarabidae); e Acanthocinus obsoletus # 107 for each insect The average burst duration, pause (Cerambycidae); f and g Enaphalodes rufulus /4 104 (Ceramby- duration and interburst interval were 79_+24 ms, cidae); h # 102 female (Mutillidae); i D. 92 _+ 62 ms and 166 _+ 68 ms, respectively. Representa- occidentalis # 105 male; j D. lepeletierii # 136 female. Last (over- tive histograms of burst duration and interburst inter- flow) bin in each histogram shows number of counts of intervals longer than 4.8 ms val are shown in Fig. 4. About 75% of the distribu- tions of burst duration, pause duration and interburst interval showed positive skewness. In addition, except for pause duration and interburst interval [Fig. 4c]). for Tropisternus and Hybosorus beetles (Figs. 3e, f, I attribute the generally lower variability of Tropis- and 4c, d), the coefficient of variation C was high, ternus and Hybosorus to lack of close coupling be- ranging from 0.29 to 2.15, indicating that the tempo- tween struggling movements and stridulatory move- ral structure of the stridulation is rather arrhythmic. ments in these beetles. In general, an insect stridulates Markl et al. (1977) and Markl and H611dobler (1978) because it is restrained in some way, and as a result report somewhat lower variability for the burst dura- most insects are simultaneously both stridulating and tion and interburst interval of ant disturbance stridu- vigorously struggling to free themselves. Usually, the lation; C calculated from their data ranged from 0.13 mechanics of stridulation are such that the spasmodic to 1.00. However, the authors felt that their method body movements involved in struggling, including at- underestimated the variability of these sounds. tempts to sting or bite, disrupt the rhythmicity of Tropisternus and Hybosorus generally showed less stridulation. However, in Tropisternus and Hybosorus, variation than the other species studied, with C< 0.23 both of which employ an abdominoelytral method (although one individual showed higher variability of stridulation (Dumortier, 1963a), struggles are es- W.M. Masters: Insect Disturbance Stridulation 263 A.I. _ m,i, Jl.li, lhirL.=..,....,~....li.i.d.L~..J,l,=,~.-.= :nll e

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Fig. 3a-i. Oscilloscope traces of 5-s portions of disturbance stridu- 20 t -I " ' P lations of various insects, a Omophron labiatum/4 115 (Carabidae) ; b Monochamus titillator ~/101 (Cerambycidae); e Acanthocinus no- dosus/4 103 (Cerambycidae); d Enaphalodes rufulus H 104 (Ceram- O; bycidae); e Tropisternus collaris /4 118 (Hydrophilidae); f Hybo- 40" jf 20 sorus illigeri ~ 117 (Scarabidae); g and h Dasymutilla occidentalis ~/105 male (Mutillidae) ; i D. lepeletierii # 136 female. Traces dark- ened by hand for good reproduction of amplitude envelopes 20 , 0

sentially limited to flailing the legs; the slight stridula- tory movements of the abdomen agaiffst the elytra 260 460 ; o z6o 400 are not greatly affected by the insect's exertions. Fur- .msec ther support for the contribution of struggling to the Fig. 4 a-j. Frequency histograms of burst duration (lower histogram erratic nature of disturbance stridulation is seen in in each pair) and interburst interval (upper histogram). The insects Fig. 3, where the sound of a struggling mutillid wasp (a through j) are the same as in Fig. 2. Values in each bin are percentages of total number of observations. Last bin in each (trace g) becomes much more regular during a pause histogram: number of intervals longer that 0.5 s in its struggles (trace h). Some insects may emit sound only when the scra- per moves in a particular direction over the file and sounds of different insects by t-tests revealed many not on the return stroke. However, other insects evi- statistically significant differences. However, there is dently produce sound on both strokes, as can be seen some question as to whether predators could use these in Fig. 3 a and d, where the amplitude of the sound differences to identify particular insect species, since is different on the fore- and backstrokes. For a few individuals of the same species often produced sounds insects, one or more temporal measures also exhibited with different temporal characteristics. Even the stri- bimodal distributions (e.g., Fig. 2g), as one would dulation of the same individual varies from time to expect might result from back and forth movement time, as shown by burst duration and interburst inter- of the scraper. However, for most insects, separation val for the disturbance sound recorded from the same of two modes was not observed, either because the insect on two different days in Fig. 4f and g. The modes fell too close together, or because the irregular- difference between the means for burst duration and ity of the stridulation caused too much overlap be- for interburst interval are both highly significant (t= tween them. 7.7, dr=210 and t=7.5, df=145 respectively, Comparison of the temporal parameters of the P<0.001 for each). 264 W.M. Masters: Insect Disturbance Stridulation

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Fig. 6a-]. Averaged airborne sound spectra for individual insects 50 kHz I00 with background noise subtracted as described in Methods. Insects a through j the same as in Fig. 2. Small dots connected by solid Fig. 5a and b. Airborne sounds (insets) and power spectra for lines represent measurements significantly (P<0.05) above back- disturbance stridulations of two representative insects. Bar below ground noise. Readings not significantly above noise connected each spectrum: approximate region where the signal power is above by dashed lines. In l, the average level of the background noise, background noise power. Vertical axis in dB re 20 x 10-6 Pa. a which was the same for all spectra, shown as a dotted line Acanthocinus obsoletus/4 107 (Cerambycidae) recorded at a distance of lcm. Peak pressure level measured from the airborne sound waveform: 89 dB ; rms level (2 ms integration time) : 72 dB. b Dasy- mutilla occidentalis //102 (Mutillidae) recorded at a distance of 3 cm. Peak pressure: 88 dB; rms level: 70 dB

Spectral Analysis - Airborne Sound The most important feature of the power spectra of disturbance sounds is their typically wide frequency The airborne component of disturbance sounds is coverage For instance, the frequency limits at which composed of transient changes (impulses) in sound the power in the spectrum shown in Fig. 5 a drops pressure resulting from each impact of the scraper below the background noise power are about 5 and against a tooth of the file. Figure 5 shows typical 60 kHz, a bandwidth of 55 kHz. Because power spec- power spectra derived from the pressure waveform tra for an insect's disturbance sound varied from mo- (insets) for portions of the disturbance sound of two ment to moment, and because the background-noise insects. The small peaks in the sound spectra regularly limits of the sound are difficult to determine, spectra spaced at about 1-kHz intervals are determined by were averaged and background noise subtracted Fig- the tooth-strike rate; the frequencies at which they ure 6 shows averaged spectra for representative in- occur are integer multiples of this rate, as would be sects. For the 42 insects analysed, the average lower expected for a periodic waveform. The '~more perio- frequency at which the sound power was significantly dic" the waveform by which I mean the more reg- (P<0.05) above background noise power was ular the time interval between impacts - the more 2.6+ 1.0 kHz, and the average upper frequency was easily the small peaks can be distinguished, within 76_+2.1 kHz. Of course these limits depend greatly the limitations imposed by the frequency resolution on the intensity of the sound relative to background of the analyser. This can be seen in Fig. 5 by compar- noise, so a better measure, nearly independent of sig- ing a (regular tooth-strike interval) with b (less regular nal-to-noise ratio, is the 10-dB bandwidth, which is interval). determined by the most distant points on the spec- W.M. Masters: Insect Disturbance Stridulation 265

trum at which the average power is 10-dB below the level at the frequency of maximum power. The aver- 50, age 10-Bd bandwidth was 39 + 17 kHz, with the aver- age center of the 10-dB bandwidth at 25-+11 kHz. The average frequency of maximum power was 20-+ 10 kHz. 30 The disturbance sounds described here were not very intense. The maximum rms sound pressure of individual insects ranged from 14 to 61 dB re 20 x 10 -6 Pa, measured between 0.5 and 100 kHz at I0 a distance of 10 cm (as computed from the pressure measured at 0.5 to 5 cm). These readings were ob- tained with a 2-ms integration time, although for mammalian and avian ears, the effective time constant 50 is probably longer than this (Ehret, 1976; Dooling, 1979). For impulsive sounds, such as disturbance stri- dulation, a longer integration time would reduce the measured rms pressure (Skovmand and Pedersen, 1978). The peak pressure ranged about 15 to 20 dB 30 higher than the rms level.

Spectral Analysis - Cuticular Vibration

I0 Cuticular vibration records, such as those shown in Fig. 7, were obtained from 26 insects. Spectra were dB i i i not averaged because usually only one or a few brief vibration recordings were obtained for each insect. 50- This was because I had difficulty keeping the strug- gling in the sensitive region of the vibration 0 I msec 20 detector, and because insects did not always cooperate by stridulating at just the right times. For each insect 30 I selected one vibration recording with good signal-to- noise ratio for detailed analysis. The maximum vibra- tion amplitude averaged 4.2_+2.7 ~tm peak to peak. Values for individuals ranged from 1 to 10 ~tm, but IO these amplitudes must be regarded as correct only to about ___ 3 dB, since the calibration signal of the I I I I I I I I I i i vibration device was not always capable of tracking d the rapid fluctuations in the instrument's responsive- 50- ness as the insect changed position. (Increasing the surface area measured by the device, ~0.14 mm 2 in this study, would have made it easier to record vibra- tion and also improved calibration tracking, but I 30 originally thought that this might lower the frequency response of the detector by phase cancellation of the high-frequency vibrations.) Most of the energy of vibration is found at lower I0 frequencies than in the airborne sound. The above- noise bounds of the vibration signal averaged I I I I I 1 t I I 0.5+_0.3 kHz to 7.0_+2.6 kHz, compared with 2.6 to 0 I0 kHz 20 Fig. 7a-d. Power spectra of vibrations recorded from four insects. # 128 (Scarabidae); b Tropisternus collaris/4 124 (Hydrophilidae); Vibration waveform shown in insets. (Outward direction relative c Enaphalodes rufulus /4 104 (Cerambycidae); d Dasymutilla occi- to the insect is upward.) Bar below each spectrum: approximate dentalis/4 102 (Mutillidae). The maximum peak-to-peak amplitudes region where signal power is above background noise power. Verti- for the vibrations in a, 5, c and d are approximately 6.8, 7.6, cal axes in dB with arbitrary reference level, a Hybosorus illigeri 2.4 and 1.8 ~tm, respectively 266 W.M. Masters: Insect Disturbance Stridulation

76 kHz for airborne sound. The mean frequency of Taken together, these cues might provide the basis maximum vibration power was 1.3 _+ 0.6 kHz, falling, for a mimetic resemblance among disturbance sounds. on average, by 11_+7.4 dB at twice this frequency. However, the disturbance sound of a particular insect Based on this rate of decline, the average 10-dB band- may not display all of these characteristics. Further- width for vibration, which was not measured because more, no one of these features is, by itself, unique vibration spectra were not averaged, must be less than to disturbance sounds; no single feature will discrimi- a few kilohertz, compared with an average 39 kHz nate disturbance stridulation from other types of in- for the airborne sound. sect sound. This is hardly surprising, though. Types The frequency of maximum vibration power ap- of sound are distinguished by context, e.g., distur- pears to be determined by the tooth-strike rate, as bance, calling, courtship, etc. (Alexander, 1967), and can be seen in Fig. 7 a and c where tooth strikes occur some insects may emit identical or nearly identical with sufficient regularity to produce an obvious peak sounds in more than one situation. Mutillid wasps, at the tooth-strike rate (frequency). The previously for example, stridulate during courtship in a manner determined average tooth-strike interval (1.1 _+ 0.5 ms) similar, if not identical, to their manner when ~corresponds to a rate between 0.6 and 1.7 kHz, cer- disturbed (Spangler and Manley, 1978). tainly in the same range as the frequency of maximum Undoubtedly, the similarity of the sounds de- vibration power. scribed in this study is enhanced because they are One insect (~/104, Enaphalodes rufulus: Ceramby- all produced by a file-and-scraper mechanism. One cidae) was studied in somewhat greater detail than might argue that all resemblance among them is the others. For this insect, the vibration waveform strictly attributable to the constraints imposed on varied a good deal from point to point on its surface, temporal and spectral characteristics by the mode of but even at a single point, the vibration changed from production - the sounds are alike because they are burst to burst. In fact, change in the cuticular vibra- all produced in the same way. This may be true of tion waveform from burst to burst was characteristic the basic burst/pause pattern. Nevertheless, the exis- of all insects. The common feature of cuticular vibra- tence of sounds produced through a file- and-scraper tion seems to be a rapid reversal in direction of device but with quite different spectral properties, movement on one half of the cycle (usually the inward such as the calling songs of most gryllids, which are to outward change) and a more gradual change in the very narrowband and nearly pure tones (Alexander, other direction (outward to inward). The result is a 1962; Dumortier, 1963b), demonstrates that the sharply peaked waveform, often appearing scalloped sounds are not completely constrained by the prop- like a rectified sinusoid, such as seen in Fig. 7 a. erties of the file and scraper. Likewise, many distur- bance sounds not produced by such an arrangement still resemble those described here. For instance, the cockroach Gromphadorhina produces an intermittent, Discussion noisy, broadband hiss by forcing air through special- ized spiracles (Dumortier, 1965 ; Roth and Hartmann, On the basis of the physical characteristics of distur- 1967; Nelson, 1979). The death's-head hawk moth, bance sounds presented here, can these sounds be Acherontia atropos, emits a broadband squeak by ex- regarded as mimetic? That is, would predators per- pelling air through its proboscis when handled (Bus- ceive them as being similar ? Ultimately, this question nel and Dumortier, 1959). Likewise, arctiid moths must be answered by experiment; however, four fea- and produce broadband clicks by a buckling tures of the sounds might be used as cues by preda- tymbal mechanism (Alexander, 1960; Fullard et al., tors: (1) The pattern of the sounds is simple - bursts 1979). separated by pauses. Bursts are about 80 ms long As in the examples just given, broad bandwidth and occur at a rate of about 5-10 per second. (2) seems to be a nearly universal feature of insect distur- The sounds are irregular (Haskell [1974] describes bance sounds (Haskell, 1961). Wide spectral coverage them as 'unpatterned'). The coefficient of variation makes them noiselike - more like a hiss than a whistle. for tooth-strike rate, burst duration, pause duration Outside of , many additional examples can and interburst interval is usually >0.30. (3) The be given of noiselike sounds produced by animals sound pressure waveform is impulsive. Consequently, in defensive situations (Cott, 1940): the hiss of cats the frequency span is very broad, the 10-dB band- and snakes, the rustle of porcupine quills, and the width averaging about 40 kHz. (4) The cuticular vi- buzz of rattlesnakes, to name only a few. The broad- bration has a sharply peaked waveform and contains band nature of disturbance sounds could have evolved maximum energy around 1 kHz (the tooth-strike to permit the sounds to be perceived~ by a gamut rate). of adversaries whose optimal hearing ranges do not W.M. Masters: Insect Disturbance Stridulation 267 coincide. Thus, whether the predator is a whose tify regarding them as mutually mimetic. In this event, sensitivity to airborne sounds is probably greatest be- predators may react similarly to different insects that low a few kHz (Frings and Frings, 1966 ; Barth, 1967), produce disturbance sounds when attacked. This or a small mammal whose optimal frequency range should be tested experimentally, but if true, it follows probably lies far above that of (Masterton that the communicatory interchange in some preda- et al., 1969; Ehret, 1977), the disturbance sound will tor-prey confrontations may be more complex than provide energy in the range appropriate for the preda- commonly recognized. Since many insects with a dis- tor. turbance sound also possess a potent defense (Pocock, A potential problem arises in explaining sound radi- 1896 ; Marshall, 1902; Cott, 1940; Eisner et al., 1974), ation by stridulating insects. Cuticular vibration, the one function of the sounds may be as an acoustic source of the airborne sound, contains little energy warning to attacking predators. The meaning at high frequencies, yet it is at these frequencies that conveyed is not simply a querulous 'Let me go,' but insects radiate maximum energy into the air. Precisely a rather more menacing 'Let me go or else!' But this discrepancy between cuticular vibration energy the 'or else' may be bluff; the mimicry may be either and radiated energy was foreseen and discussed by Batesian or Mfillerian. Consequently, the predator Markl (1968) when he considered sound radiation need not, and probably ought not, respond to the by stridulating ants. Sound radiation is most effective sound by immediately retreating. The interaction may when the dimensions of the sound source are larger instead proceed through stages of gradually increasing than about a third of a wavelength (Kinsler and Frey, conflict to its ultimate outcome, when either the pre- 1962; Michelsen and Nocke, 1974). The insect's sur- dator breaks off its attack or else the insect is sub- face vibration has most of its energy near 1 kHz, dued. These ideas are developed more fully in another but because the insect is so small, it is a very poor paper (Masters, 1979 a). sound radiator at this frequency. The vibration energy at 20 kHz is comparatively slight (in fact, at this fre- quency vibration energy was not detectable because Supported in part by an NSF predoctoral fellowship and Bache Fund stipend from the National Academy of Sciences (Masters), it was below the background-noise level of the mea- and NIH grant AI-02908and NSF grant PCM77-25807 (T. Eisner). suring instrument), but at this frequency the insect I thank the insect identification service of the U.S. Department is an effective sound radiator. Given some hypotheti- of Agriculture and E.R. Hoebeke for identification of insects. I cal (but probably reasonable) values, if the amplitude am grateful to the Director and staff of the Archbold Biological of vibration at lkHz is 0.5gm and at 20kHz is Station, Lake Placid, Florida, for their hospitality while I was there. To my chairman, Dr. Thomas Eisner, I wish to acknowledge 0.005 gm, then the sound pressure measured at a dis- my great debt for his original proposal that I study insect distur- tance of 1 cm will be about 12 dB greater at 20 kHz bance sounds and the suggestion that the sounds might be mutually than 1 kHz (Masters, 1979c). These calculations are mimetic, and for his unfailing support throughout my graduate based on a model of the insect as a radially pulsating, career. I also thank Drs. Eisner, R.R. Capranica, D.J. Aneshansley, spherical sound source 3 mm in diameter (for discus- W.L. Brown and J. Camhi for helpful criticism of the manuscript, Drs. Capranica and G. Hausfater for loan of equipment, and Dr. sion, see Markl [1968] and Masters [1979c]). A. George for discussions of acoustics. Finally, for invaluable help The question remains, though, as to why there with all phases of this research, I thank my wife, Anne Moffat. should be so little overlap between the energy spectra of the insect's airborne sound and that of its surface vibration. Maximum efficiency would seem to de- References mand that the airborne and vibrational energy be matched. But in the present case, 'inefficiency' brings Alexander, R.D. : Sound communication in and Cica- a bonus - the disturbance sound becomes a more didae. In: sounds and communication. Lanyon, W.E., effective stimulus, for the reason that receptors of Tavolga,W.N. (eds.), pp. 38-92. Washington: Am. Inst. Biol. Sci. 1960 airborne sound typically are tuned to higher fre- Alexander, R.D. : Evolutionarychange in cricket acoustic commu- quencies than vibration receptors in both vertebrates nication. Evolution 16, 443-467 (1962) and invertebrates (Autrum, 1963; Masterton et al., Alexander, R.D. : Acoustical communication in arthropods. Annu. 1969; Burgess and Perl, 1973; Schwartzkopff, 1974). Rev. Entomol. 12, 494-526 (1967) Autrum, H. : Anatomy and physiologyof sound receptors in inver- Thus the maximum energy bands in the airborne and tebrates. In: Acoustic behavior of animals. Busnel, R.-G. (ed.), vibrational components of the sound are matched pp. 412M33. Amsterdam, London, New York: Elsevier 1963 to the frequency characteristics of the receptors that Barth, F.G. : Ein einzelnes Spaltsinnesorgan auf dem Spinnentar- detect the two components. sus: seine Erregung in Abhfingigkeit von Parametern des Luft- In summary, the analysis presented here suggests schallreizes. Z. Vergl. Physiol. 55, 407-449 (1967) Bauer, T. : Experimente zur Frage der biologischen Bedeutung des that disturbance sounds do have some features in Stridulationsverhaltens von Kfifern. Z. 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