Behavioral Ecology Behav Ecol Sociobiol (1982) 11:269-281 and Sociobiology 9 Springer-Verlag 1982

Plants as Transmission Channels for Vibrational Songs

Axel Michelsen 1, Flemming Fink 1, Matija Gogala 2, and Dieter Traue 3 Institute of , Odense University, DK-5230 Odense M, Denmark 2 Institute of Biology, University E. Kardelj, , Yugoslavia 3 Institut ffir Allgemeine Zoologic, Freie Universit~it, D-1000 Berlin

Received May 24, 1982 / Accepted October 18, 1982

Summary. The vibrational songs of several species of vibration of the plant. The amplitude of vibra- of cydnid bugs and 'small cicadas' (leafhoppers tion does not decrease monotonically with distance and planthoppers) living on various types of plants from the emitter (Fig. 6). are recorded by means of laser vibrometry. The These filtering properties of the plants mean recorded vibrational songs are analysed with that it is essentially impossible to predict which respect to amplitude, frequency spectrmn and frequencies in the signals will be amplified or atten- structure in the time domain (Figs. 2-5). uated in the plant at the location of the receiving The emission of vibrational songs from singing animal. The vibrational signals recorded from the on plants is simulated. A small magnet is animals cover wide,, frequency bandwidths. The glued to the surface of the plant and moved by signals are therefore well adapted to the filtering means of an electromagnet about one cm away properties of the plants, but the signals of the (Fig. I). The vibrations are recorded by means of species studied here do not appear to be particular- laser vibrometry. The propagation velocity of the ly adapted to specific properties of the host plants. vibrations increases with the square root of fre- The muscular power needed for communica- quency, i.e. in the way expected for bending waves. tion by means of various types of vibrational The mechanical properties of plants ranging signals is calculated. The result of this calculation from soft bean plants to stiff reeds and maples supports the conclusion that the signals recorded are measured. The results are used for calculating here are carried by means of bending waves. the theoretical propagation velocities of bending The communication strategies open to small waves. The measured and the calculated values are insects are considered. Vibrational signals appear rather close (Table 1). Although the mechanical to be an efficient means of communication, but properties of the plants studied vary widely, the only certain types of signals are suited, because propagation velocities at a certain frequency are the plants cause a considerable distortion of the of the same order of magnitude (Table 1). signals. One kind of distortion, the dispersive prop- In all the plants studied, only little vibrational erty, may - in theory - be used by the listening energy is lost by friction at frequencies below some animals to obtain information about the direction kHz. Communication by means of bending waves and distance to the singing animals. is possible over distances of some meters. The bending waves are reflected with little loss of ener- gy both from the root and from the top of the plant. The vibration signals may therefore travel Introduction up and down the plant several times before decay- Airborne sound waves offer an efficient way of ing completely (Fig. 7). The vibration at a certain communication for man and many animals. The spot on the plant depends not only on the distance environment is a complicated acoustic filter, how- to and nature of the emitter, but also on the modes ever, and the sound signals therefore have to be adapted to the particular environment, in which * Dedicated to Dr. F. Ossiannilsson, whose pioneering studies the animals live (reviews: Michelsen 1978; Wiley led to the suggestion that small insects may use plants as and Richards 1978). transmission channels for their songs It is difficult for small animals to use airborne

0340-5443/82/0011/0269/$02.60 270 sounds for communication, except at short dis- Several kinds of waves can propagate in rod- tances. Small sound emitters are very inefficient shaped solid structures: longitudinal, transverse, at low frequencies (see e.g. Michelsen and Nocke torsional, bending, and (in thick rods) surface 1974), and ultrasonic signals are not suited for pen- waves. The longitudinal waves are analogous to etrating an environment dominated by plants (Mi- sound waves, where the particles vibrate in the di- chelsen and Larsen, in preparation). Vibrational rection of wave propagation, but for this and other signals, on the other hand, appear to be a better structure-borne waves the displacement of a choice. For physical reasons, animals living in or certain part of the rod from its equilibrium posi- on water or solid media (soil, wood) may efficiently tion is associated with a tensile stress. The tensile emit vibrational signals at low frequencies, where stresses are here in the direction of wave propaga- little airborne sound can be produced (Markl tion. Pure longitudinal waves do not occur in rods, 1968). because local changes in length are associated with The existence of vibrational communication changes in cross-section. In such quasi-longitudi- has been demonstrated by means of behavioural nal waves the ratio (R) between the transverse and observation in several groups of insects (Markl longitudinal displacement amplitudes is 1973; Gogala et al. 1974; Cokl et al. 1978; Str/ib- ing 1977; Bell 1980). Most of the signals are related R = 2z~Izr/2L (1) to sexual behaviour. The range of communication where rc is 3.14 ..., r is the radius of the rod, 2 L may be limited to a few cm in heavily damped is the longitudinal wavelength, and g is Poisson's media like soil, but ranges of 0.8-2 m have been ratio (which is around 0.2-0.3 for most materials). reported for small insects living on plants (Chvfila The velocity of propagation (%) is determined by et al. 1974; Ichikawa 1976, 1979). The methods Young's modulus of elasticity (E) and the density used in most of the earlier studies have been re- of the material (p) stricted to, for example, observing the behaviour of animals sitting on the same plant or on neigh- bour plants. The vibrational signals have been c L = (2) measured either with vibrational transducers (grammophone stylus, accelerometer) or as weak Transverse waves ('rotational' waves) and tor- airborne sounds with condenser microphones. sional waves are closely related, and both propa- These methods did not allow detailed measure- gate with a velocity which is about 60% of c L. ments or a determination of the kind of vibrational The motion of the material and the direction of waves used by the animals. The exceptions known the tensile stresses are here in a plane perpendicular to us are the pioneering studies of the vibrational to the propagation of the wave. Transverse waves signals of ants buried in the soil (Markl 1968) and may occur in large plates, but no component of of plecopteran signals transmitted through plants the movement is perpendicular to the surface. The (Rupprecht 1968). The results of the latter study same is true for torsional waves travelling in rods are discussed in detail in this article. with a circular or annular cross-section. Compo- Vibrations in the nm range may be measured nents of motion normal to the surface only occur within a broad frequency range by means of laser in beams with non-rotational cross-section. vibrometry (Michelsen and Larsen 1978). The laser Bending waves (' flexural' waves) are sometimes beam does not load the plant mechanically, and termed 'transverse' waves, but this is not the defi- the vibrational signals can therefore be detected nition of transverse waves in the strict sense used without any interference from the measuring sys- in this paper. The propagation of bending waves tem. In this article we report measurements of the is complicated by being dispersive (frequency-de- vibrational songs of several species of small insects pendent). Furthermore, for short pulses of sinusoi- (cydnid bugs and 'small cicadas') on a variety of dal carrier wave (of frequency f) one has to distin- plants with rather different physical properties. We guish between the propagation velocity of the car- further describe experiments and calculations, rier wave (the phase velocity, ca) and that of the which were carried out in order to elucidate the pulse envelope (the group velocity, Ca, which is nature of the vibrational signals and the filtering twice %). % is given by properties of the plants. j- Basic Physics of Waves in Beams cB = Vco (3) The physics of structure-borne vibration is rather complicated. A detailed introduction is given by where I is the (surface) moment of inertia, m' the Cremer et al. (1973). mass per unit length, and co = 2 zcf 271

I is proportional to the fourth power of the beam substrates. In this study we measured the premating songs from radius (r) and m" to the second power of r. males and females both on dry beech leaves and on the stems c B is therefore proportional to the square root of of Galeobdolon vuIgare. r and to the square root of f. The power flow The Vibrational Songs. The vibrations were measured with a is made up of a force contribution and a moment laser vibrometer. The use of this instrument for vibration mea- contribution, which are totally out of phase and surements has been described in detail (Michelsen and Larsen of equal magnitude, so that the power flow is con- 1978). In brief, laser light is focussed at a spot of 30 gm diame- ter on the surface of the plant. Vibrations of the plant in the stant everywhere at all times. Like other waves, direction of the laser beam causes Doppler-shifts in the fre- the bending waves are reflected whenever there is quency of the reflected light. The output voltage of the instru- a change of impedance along the beam. At branch- ment is linearly related to the instantaneous vibration velocity ing junctions a part of the wave energy may also over a broad range of amplitude and frequency. The lower be transformed into a longitudinal wave. limit of detection without averaging or filtering of the output signal may be at vibration amplitudes of about 1-2 nm, if Various surface waves (Rayleigh, Love) as well the plant has ideal reflection properties for the laser light. A as shear and compressional waves may propagate good reflection was obtained in these experiments by painting along the surface of a solid medium when the ge- small areas on the plant with white correction fluid (Tipp-Ex). ometry of the medium is not restricting the wave The extra mass added in this way was extremely small in com- motion to one or two directions (as in beams and parison with the mass of the plant. The behaviour of the animals and their position on the plates), see e.g. Ewing and Press (1956). The situa- plant were noted during the recordings. Airborne sounds were tion may be very complicated if the medium is occasionally recorded at a few cm distance by means of a 1" not homogeneous (cf. the spreading of seismic condenser microphone (Briiel & Kja~r 4131) connected to a waves). Surface waves are unlikely to play any role preamplifier and measuring amplifier (Briiel & Kj~er 2919 and 2607). The analog output signal from the laser vibrometer and in the problems considered here, but they may the signal from the microphone were stored on tape (Hewlett perhaps be relevant in the transmission of, for Packard 3960) for further processing. Oscillograms were made example, vibration signals in the stems of thick in the conventional way, and sonagrams with Kay sonagraphs trees. (606~B and 7030A) operated without automatic gain control. Frequency analysis was also performed with a spectrum ana- lyser (Hewlett-Packard 3588A) and with a digital computer (PDP 8/e). Materials and Methods Mechanical Properties of the Plants. The mechanical properties The Plants and Animals. The plants studied include the host of pieces of plant stem were determined in the following way. plants of the insects whose vibrational songs have been mea- Young's modulus of elasticity (E) was obtained by clamping sured and were further selected so as to represent a wide spec- a slim piece of stem at one end and deflecting the other end trum of physical properties (flexural stiffness, inertia, and perpendicular to its long axis. The force needed for obtaining mass). We studied the following plants: Viola faba L. (broad a certain deflection was measured with a force transducer bean), Thesium bavarum Schrank, and T. divaricatum Jan (toad- (DISA51 D17) coupled to a reactance converter (DISA 51 flax, herbs), GaleobdoIon vulgate (Pers.) (= Lamium galeobdo- E01). Young's modulus was then calculated by means of the Ion, yellow archangel, a herb), Phragmites communis Trin. equation (Cremer etal. 1973) (reed), Phalaris (Baldingera) arundinaeea L. (reed-grass), Aver pseudoplatanus L. (maple) as well as the dry leaves of Fagus E= F13/3 dI (4) silvatiea L. (beech). where F is the force, l the length of the stem, and d the deflec- Three species of' small cicadas' were studied. Euscelis lineo- tion. The (surface) moment of inertia (1) was calculated from latus Brulle is a polyphagous leafhopper living on different measured dimensions of cross-sections of the stem (see e.g. species of trefoil and on lucerne (Medicago sativa L.). The Alonso and Finn 1972). Finally, the mass per unit length (m') insects were collected in the district of Eifel, FRG, and main- was obtained simply by weighing wet pieces of stem. tained in culture in the laboratory on bean plants. The polypha- A rough measure of the internal (frictional) damping at low gous leafhopper Euscelidius variegatus KBM feeds on various frequencies was obtained by fastening pieces of stem at one plants, e.g. barley and various species of cabbage. This species end and measuring the decaying vibrations following small de- was obtained near Heidelberg, FRG, and maintained in. culture flections of the opposite end with the laser vibrometer. on bean plants. The planthopper Euides speciosa Boh. is mono- Artificial vibrations were induced in the plants by gluing phagous and feeds on reeds. This species was collected in Berlin a small magnet (about the same weight as the bugs: 25 rag) and maintained on reed in the laboratory. to the surface of the plant and vibrating it by means of an Four species of cydnid bugs were studied. Sehirus (Cantho- electromagnet about one cm away (Fig. 1). For certain types phorus) impressus Horvath, S. (C.) dubius Scopoli and S. (C.) of experiments the plants were vibrated by direct contact with melanopterus H.S. are only found on different species of the tip of a cone-shaped rod fastened to a vibration exciter Thesium. The animals and plants were collected in , (Brfiel & Kj~er 4810); this method of vibrating the plant cannot Yugoslavia. A fourth species of bug, Sehirus (Tritomegas) be used for all types of measurement, since the rod restricts bicolor (L.) feeds on different plants, preferably on different the movements of the plant. Two kinds of artificial vibrations species of Lamium. The animals hibernate as adults, and in provided the most reliable information: short, filtered sine the spring the courtship and mating occurs in the hibernation waves and continuous sine waves with constant or slowly places on dry leaves, on soil, etc. The adults of the second changing frequency. generation court and mate on different Lamium species. These The short, shaped sine waves were used for measuring the animals are therefore able to communicate on widely different propagation velocity and for illustrating the reflection of vibra- 272 I trigger

function generator spectrum signal Ii rape-recorder i analyser averager i . {/+k, 20 bit) ~----~ x-y recorder J -- i t / "-~- passaa"d- l I I I I i ' I vibromefer I control + 4, PhaSefrolCOn- I

I I ( I I I

NUalur ma~ner

( ..... ). Connections common to both experiments are indicated in full line. Further explanation in the text

tion waves from the ends of the plants. The set-up for these phase velocity and the group velocity. The phase of the wave experiments is shown in Fig. 1. A function generator (Exact - and thus its shape - changes as the wave propagates along 128) produced a single sine wave, which passed a band-pass the stem. One may therefore obtain quite erroneous results, filter (Krohn-Hite 3550, slopes 24 dB/octave; -3 dB point of if one is measuring, for example, the time elapsed to a maximum both filters at the frequency of the sine wave). The phase angle deflection at a point along the stem. One may avoid this prob- of the shaped sine wave could be varied with a home-made lem by recording the wave shape at many different phase angles phase control unit. The resulting pulse, which had a reasonably both at the point of origin (the position of the magnet) and narrow frequency spectrum, was then amplified and sent to at points some distance from the point of origin. The time the electromagnet. The signal from the laser vibrometer was difference between the envelopes of the families of curves displayed on an oscilloscope and stored in the memory of a (Fig. 7) obtained at the different points then indicates the group digital averager (Nicolet 1170). A number of signals (e.g. 16 velocity of the vibration wave. or 32) were added, and the averaged signal was displayed on a X-Y recorder (Briiel & Kjmr 2308). A continuous sine wave with a slow change in frequency with time was used for determining the frequency filtering of Results vibrations travelling from one spot to another (Fig. i). A spec- trum analyser (Hewlett-Packard 3588A) produced a sine wave, The Vibrational Songs e.g. sweeping from 100 Hz to 5.1 kHz in 10 s, which was used and Their Transmission in Plants for vibrating the plant either through the electromagnet or through the vibration exciter. The signal from the laser vibro- Vibrational songs were recorded from four species meter was sent back to the spectrum analyser, in which various of cydnid bugs and three species of' small cicadas', constant bandwidths could be selected. The duration of the sweep, the frequency range, and the filter bandwidth were ad- while the animals were on their natural substrates. justed to allow sufficient time for analysis. The spectrum thus From the bugs we recorded courtship songs, rival- produced was sent to the signal averager, and the averaged ry songs, and female acceptance songs; from the spectra were stored on a digital tape recorder (Penny & Giles ' small cicadas' calling songs and alternation (c~ - 2100). After the experiment, the spectra were transferred to the signal averager for further processing. or c?- ~). For the behavioural significance of these When measuring propagation velocities one has to take into signals see Gogala et al. (1974), Ichikawa (1976) account that bending waves propagate with two velocities, the and Striibing (1977). 273

The amplitude of the songs varied greatly, but the vibration velocity normal to the surface of the plants was between 0.1 and 1 mm/s in most record- ings from plant stems and leaves and between 0.3 and 2 mm/s in most songs recorded from the dry leaves. All the signals emitted by the bugs and 'small cicadas' studied here cover broad frequency ranges, but the microstructure of the signals differ. In many cases we made simultaneous record- ings of the vibrational signals in the plants and of the weak airborne sounds emitted by the ani- mals. In the "small cicadas" the frequency range of sounds and vibrations is almost identical, but the main energy is emitted at lower frequencies in the vibrational signals. For example, the air- borne sounds are a maximum at about 550 Hz in Euides speciosa (Traue 1978b), whereas the vibra- Fig. 2. Alternation betweenmale and femalein the small cicada Euides speciosa. The vibrational songs were recorded about tional signals are most intense around 150-250 Hz 10 cm from the animals, which were singing on a reed stem (Fig. 2). In the bugs the low-frequency vibrations about 3 cm from the soil. Sonograph bandwidth 37 Hz. Note produced by the tymbal mechanism are found both that the dynamicrange of the sonograph is only 20 dB (a factor in the weak airborne sound and in the vibrational of 10) songs. The stridulatory components of the songs, however, cover different frequency ranges in air quency range covered, but concentrated in fre- and in the plants. In air, the sound energy extends quency bands. This is true both for the very short to at least 12 kHz, and the main energy is emitted 'clicks', for the 'croaks', and for the long calls at 3-4 kHz (Gogala et al. 1974). In contrast, the (Figs. 2 and 4). As illustrated in the figures, the plant vibrations are below 2-3 kHz, and the main position of the frequency bands of maximum vi- energy is below 1,500 Hz and in most cases below bration amplitude may vary (cf. the male songs 500 Hz. The vibrational songs also contain compo- to the left and right in Fig. 2), and the frequency nents which do not occur in the airborne signals. bands contributing to the short clicks are not the Opening or closing of the wings, movements of same as those of the long-lasting calls (Fig. 4). The legs, etc. give rise to low-frequency vibrations reasons for this are not obvious (see Discussion), which are transmitted along the plants in the same but the spreading of the signal energy over such way as the 'real songs'. It is possible that such a broad frequency range means that there is always vibrations also carry information of relevance for some vibration coming through to the 'listening' the animals. animals. The mechanism responsible for the emission of The long-lasting calls (Figs. 3 and 4) are com- vibration signals in the 'small cicadas' is not un- posed of some hundred impulses. The time interval derstood, but it appears to be very different from between these impulses determines the basic fre- the well-known tymbal mechanism in real cicadas. quency component of the call. In most songs, the The basic unit in the signals is the impulse, which harmonic components number 2 or 3 are the most typically lasts a few ms (Fig. 3 A). The animals can intense (but see the lower example in Fig. 4). The emit single impulses, but more often they emit a intervals and harmonic frequency components are series of impulses. A short series of impulses (which not constant. As illustrated in Fig. 4 there is a in behavioural papers is called a 'click', but which gradual decrease in frequency to about 85% of really is an impulse train) may last for 10-15 ms the original value over the first 90% of the dura- (e.g. in Euides speciosa, Fig. 2). A somewhat longer tion. During the last 10% of the duration, the fre- series may last about 50 ms and constitutes a quency drops rapidly to reach about 65% of the croak-like signal (e.g. in the calling song of Eusceli- original value at the end of the call. The males dius variegatus males). A much longer series con- of another species, Euscelis ononides occasionally sisting of some hundred impulses makes up the produce even longer calls (lasting up to 3.5 s). long calls characteristic for the calling song of, for Here, the frequency decreases gradually over the example, Euscelis lineolatus (lower part of Fig. 3). duration of the call to about 75% of the original For all these signals it is apparent that the value. During the calls, the amplitude of each of signal energy is not evenly distributed over the fre- the harmonic components varies (Fig. 4), but some 274

Fig. 3A-E. Vibrational call made by a male Euscelis lineolatus on a bean plant, recorded at 14 cm distance. This figure should be compared with Fig. 4. A Two impulses followed by short, low- frequency vibrations. B Movements of the wings just before a long call. C A part of the beginning of a long call. D Middle part of a long call. E End of a long call. Omitted from A to B:65 ms; B to C: 165 ms; C to D: 250 ms; D to E: 150 ms

Fig. 4. Impulses and long calls from Euscelis lineolatus males Fig. 5. Vibrational courtship song (type M 2, Gogala 1969) of on a bean plant. The animals were sitting on the stem a few a male bug Sehirus bicolor on a dry beach leaf. Note the fre- cm from the soil, and the vibrational songs were recorded 23 cm quency sweeps in the tymbal vibration signals (7) and the differ- (upper) and 11 cm (lower) away. Sonagraph bandwidth 150 Hz. ent frequency band covered by the stridulation signals (S). Son- Note that the dynamic range of the sonagraph is only 20 dB agraph bandwidth 37 Hz (a factor of I0) harmonics are always available for carrying the creases 3040% during a tymbal call (Fig. 5). Be- signal. tween these calls this bug produces short, broad- The bugs of the family Cydnidae have a rich band stridulatory vibrations. Some other songs of repertoire of vibration signals which are produced this bug are purely stridulatory. The stridulation by means of tymbal and stridulatory organs signals may be series of rather short clicks, or they (Dra~lar and Gogala 1976; Gogala 1970). The vi- may be croak-like (cf. the small cicadas). The brations produced by the tymbal organs are of croak-like signals (male song type 2, Gogala 1978) rather low frequency, and the frequency changes of S. impressus have a total duration of about with time. In the male courtship song type 2 300 ms and are composed of four pulses. (Gogala 1969) of Sehirus bicolor the frequency in- Most recordings were made at distances less 275

(ram/s) v 0.7-

0.6-

0,5-

0,4-

0,3 I I IIi I 0,2- Ii I -r ii IiI Iit I i 0,1- T

d 1'0 2'0 30"6 1'o 2'o Distance to the singing animal ( cm ) Fig. 6. Maximum peak-to-peak vibration velocities of songs recorded on bean plants at various distances from singing males of the small cicadas Euseelidius variegatus (left) and Euscelis lineolatus (right)

Table 1. Some examples of measured and calculated group propagation velocities (CB, in m/s) from stems of plants of widely different mechanical properties. I (surface) moment of inertia (in mr E Young's modulus of elasticity (in N/m2). m' mass per unit length (in kg/m). - not measured. Note that the propagation velocity increases with the square root of frequency. The values indicated here are from 'typical' stems. The values for individual stems varied (E and I: ___a factor of 3; m' and CB: +_10-20%)

Plant I E m' Calculated Measured

200 Hz 2 kHz 200 Hz 2 kHz

Vieiafaba 2.10- xo 4.106 9-10- 3 39 122 36 120 Galeobdolon vulgare 3-10-12 2-108 5" 10- 3 42 132 45 143 Thesium bavarum 6. ] 0-1 s 109 3' ] 0- 3 47 150 40 162 Phragmites cornmunis 4.10-11 3" 10 s 8" 10- s 78 246 75 220 Phalaris arundinacea 14.10-13 2-109 2.10-3 77 243 74 - Aeer pseudoplatanus 2,10- lo 6.109 5-10-1 88 279 95 -

than 30 cm from the singing animal. In some cases turn). The time and frequency structure of the the singing animal was so stationary that it was songs did not appear to be more distorted than possible to perform a a series of recordings at var- normally, and the vibration velocity was about ious distances. In other cases the animal(s) walked 0.1 mm/s (which in the frequency range considered around on the plant, while the vibrational songs is well above the threshold of the vibration recep- were recorded from one position on the plant. We tors, see Discussion). did not find a simple relation between the vibration amplitude and the distance to the singing animal (Fig. 6). On the contrary, the songs are often more Propagation Velocity intense at the top of the plant or on a leaf far of Artificially Produced Vibrations away, than they are on the main stern close to In Table 1, the measured propagation (group) ve- the singing animal. In a few cases it was also ob- locities in various plants are compared with the served that the songs were more intense, when the values calculated from the measured mechanical singing animal was sitting on a leaf rather than properties. The results show a reasonable agree- on the main stem. ment between the measured and calculated values In Thesiurn plants several secondary stems may of C B. The mechanical properties of the plants se- originate from one common root and main stem lected for study cover wide ranges. At one extreme, in the soil. Vibrational songs emitted on one stem bean plants cultivated in a greenhouse were so soft may spread to other stems of the same plant that they could hardly support their own weight. (Sehirus impressus singing on Thesium divarica- At the other extreme, reed and young maple are 276

rather stiff. Nevertheless, the propagation veloci- ties are of the same order of magnitude. B It should be noted that these measurements and calculations were not performed with the aim of

determining the exact values for the plants studied. I The aim was to determine the order of magnitude Ims of the different properties and to test the hypothe- sis that the waves observed are bending waves. Al- though we selected stems without branches and with as uniform a diameter as possible, one can hardly find two pieces of stem with exactly the I I same geometry. The propagation velocity varies Ims with the diameter of the stem and (in hollow stems) with the thickness of the stem wall. A statistical treatment of the data was therefore not attempted.

Physical Properties of Stems After the measurements of the propagation veloci- ties the stems were cut into minor pieces suitable for determining the values of Young's modulus (E), the moment of inertia (/), and the mass per unit length (m'). From these parameters the theo- retical phase velocity (eB) was calculated by means of Eq. 3. 10ms The rather different physical properties of the plants studied are obvious from the values listed F in Table 1. The propagation velocities do not vary much, however, partly because the velocity is only dependent on the fourth root of the values of these parameters (see Eq. 3). The internal damping was studied especially in Thesium bavarum. Pieces of stem of about 5 cm length and loaded with platicine in the free end Fig. 7A-F. The vibration of a bean plant, about 50 cm high performed 10-20 vibrations before the displace- and activated about 20 cm from ground as shown in Fig. 1. A The electrical signal (2-3 cycles of a 2 kHz sinus) sent to ment amplitude was reduced to below 5% of the the electromagnet. B The vibration of a small magnet on a initial value. We did not persue this part of the long, loose string (for comparison). C-F The vibrations mea- investigation further, but similar observations on sured on the bean plant when activated by 2 kHz pulses (C some of the other plant species also demonstrated and D) and 200 Hz pulses (E and F). C and E are at the point of stimulation, whereas D and F are from a point 3 cm higher low internal damping. on the plant. The families of curves in each of the recordings C to F were made by changing the phase angle of the stimulus. Reflections and Standing Waves Note the reflections from the ends of the plant and that the vibration amplitudes are larger in D and F than in C and E The short sine wave pulses used for measuring the propagation velocity at different frequencies had a duration of about 3 cycles (Fig. 7A). Control frequency may cause large differences in the measurements, in which the small magnet was pattern of vibration. The response of the plants glued to a freely suspended piece of string, showed resembled that expected in beams, where a vibra- that the movement of the magnet was similar to tion pulse of short duration is travelling up and the electrical signal (Fig. 7 B). The movements of down the beam several times and being reflected the plants were different, however: the short sine at the ends. That this interpretation is correct was wave pulse was repeated several times, and the confirmed in experiments where the plants were cut plant often moved for 20 ms or more after being so as to shorten the distance to the top, or where activated by a sine wave pulse of a few ms duration the short pulses were fed in at one end of the plant. (Fig. 7C-F). The pattern of movement depends Reflections occur both at the root and top of much on frequency, and even small changes in the the plant (where the impedance met by the travell- 277

dB Fig. 8. An example of the frequency filtering and attenuation of a sinusoidal vibration in the plant Thesium bavarum. Note that the vibration amplitude does ., "~176 not decrease in a monotonical manner ,.',: /\ .,,- -._.- ...... with distance for frequencies up to 1- ~''~i" iii,' W i .- ! - -. " .~. 2 kHz. 0 dB is the amplitude at the rJ 'ii | ':~ i! "., f '. l/cm position of the magnet. The distances are -20 ii "I ! ';I ! ~I I "" V~.*~...... ; \ ee*~ /"/X 4 \ approximate values. The stems of Thesium are almost solid rods with a

I I I I I circular cross-section of radius about 01 1 2 3 4 5 kHz i mm ing wave becomes somewhat larger and much magnet was glued to the lateral surface of the smaller, respectively). The reflections are normally stems. One may easily get the impression that the larger at the top than at the root (in agreement vibrations may travel as torsional waves, if one with the larger change of impedance at the top), is observing the complicated vibration of entire and the reflections may by changed by changing plants. At low frequencies one can observe very the impedance (e.g. by fastening a string to the complicated torsional movements in plants with top or by changing the soil). The occurrence of many branches and sidebranches, if one uses a reflections and the small internal damping of the stroboscope for illumination. Such torsional move- plants mean that the plants are likely to carry ments are not caused by real torsional waves, how- standing waves, when they are activated by sine ever, but by the complex geometry of the plant waves of long duration. This is indeed the case. (which may also have twisted stems). That the The standing wave patterns are often very compli- waves are bending waves and not torsional waves cated and very frequency-dependent, since the is easily shown by a measurement of the propaga- plants have a more complicated geometry than tion velocity, which is frequency dependent and simple beams. different from that expected for torsional waves. The transmission of pure tone signals in sys- tems dominated by standing waves depends on the Discussion position of both the emitting and receiving ani- mals. The transmission may be efficient, if the ani- Since the pioneering studies of Ossiannilsson (1949) mals are at the internodes, but inefficient at the it has been suspected that small insects may use nodes. The frequency filtering measured with con- their host plants as transmission channels for their tinuous sine waves with slowly changing frequen- songs. Behavioural observations have demon- cies confirmed this (Fig. 8). The vibration ampli- strated the existence of vibrational signals in sever- tude may change 10-30 dB, when the frequency al groups of insects, including Plecoptera, Neurop- of vibration changes less than 10%. This frequency tera, Coleoptera, Hymenoptera, Heteroptera and filtering was also evident in the recordings of the Homoptera (Markl 1973; Chvfila etal. 1974; natural songs at frequencies up to 1-2 kHz (see Gogala et al. 1974; Strfibing 1977). Most of the above). At higher frequencies there appears to be signals are related to sexual behaviour and allow a larger and more monotonic attenuation related the animals to attract and find a partner and to to the distance to the source. The filtering observed determine whether it belongs to the same species in different kinds of plants was of similar nature, and opposite sex. For attracting a partner, in par- and we did not detect systematic differences be- ticular, the animals have to use signals which can tween the plants studied other than a tendency for be transmitted over long distances without loosing the 'soft' types (Galeobdolon, Vicia) to be more their specific characteristics. The signals should efficient absorbers of high frequency vibrations also, if possible, carry information about the direc- than the 'hard' types of plants. tion (and distance?) to the singing animal. This study demonstrates that small insects are The Type of Waves indeed able to cause their host plants to vibrate with amplitudes 1-3 decades above the threshold The vibrations described above are bending waves. of their vibration receptors: In the cydnid bugs We added a large number of sweeps in searching we find acceleration amplitudes of 0.06-8 ms -z , for other types of waves. We did not find any evi- and the vibration receptors in these animals have dence for the existence of such waves, when the thresholds around 0.01 ms-2 (Devetak et al. 1978). 278

The vibrational songs propagate as bending waves quency components, which are in the ms-range for with only little frictional loss in energy, and they distances of a few dm. can be detected by other animals anywhere on the It is interesting that the vibration receptors and same plant (within some meters). The use of vibra- vibration-sensitive central neurons in both cydnid tional signals is not simple, however, since the and pentatomid bugs show a capacity for fre- signals may be distorted and filtered by the plant. quency analysis in the frequency range considered; Although the plants studied vary greatly in that their absolute sensitivity is sufficient for de- their mechanical properties (Table 1), the fre- tecting these frequency components in the natural quency filtering is of a rather similar nature. The songs, and that these cells respond in a phasic fash- vibrational songs are adapted to this filtering (see ion (Devetak et al. 1978; Cokl and Amon 1980). below), but we did not detect any specific adapta- It is not known, however, whether the nervous sys- tions to the properties of a specific host plant. tem is processing the time intervals between the Some species do in fact communicate on widely frequency components, or whether the animals use different substrates. For example, the bug Sehirus this possibility for locating each other in their bicolor hibernates as adult, and the courtship and behaviour. mating occurs in the spring on dry leaves, whereas the adults of the second generation court and mate The Vibrational Songs on different species of Lamium (Galeobdolon). The vibrational songs of the animals studied appear well adapted for penetrating the filter The Plants as Filters formed by the mechanical properties of the plants. In the frequency domain, the filtering appears to All the signals cover broad frequency ranges, and be due to a complicated pattern of standing waves, some of the frequency bands are therefore always which is highly dependent on frequency (Fig. 8). likely to get through to the listening animals. Both The attenuation of pure tone signals is therefore the bugs and small cicadas make short impulses dependent on the position on the plant of both or clicks, croak- like signals of medium duration, the emitting and the receiving animals. The attenu- and songs of much longer duration. In the long ation may vary up to 30 dB when the frequency signals the frequency may increase (bugs) or de- or the position of the animal(s) are changed. It crease (' small cicadas') during a signal. The fre- would therefore not be a good strategy for these quency change is 30~40% in both cases (Figs. 4 animals to use pure tone vibrational signals for and 5). The frequency sweeps are clearly audible communication. In particular, it would be difficult to humans, when the recorded signals are emitted for the receiver to locate the emitter. by a loudspeaker. It is not known whether the ani- In the time domain, the vibrational signals are mals can actually perceive these FM-sweeps. The likely to be distorted by multiple reflections from physical mechanisms responsible for the produc- the ends of the plant, which - together with the tion of the FM-sweeps are not clear either. In the small internal damping - causes short signals to long signals of Euscelis lineolatus, the time interval travel up and down the plant several times before between the impulses (Fig. 3) increases about decaying completely (Fig. 7). 30-40% during a signal. This is in nice agreement The dispersive nature of the plants when trans- with the decrease in frequency (Fig. 4). The time mitting bending wave signals also causes another intervals between the impulses correspond to the type of filtering. High frequencies travel faster than lowest harmonic frequency component. low frequencies, and the time-frequency structure It is curious, however, how the 'small cicadas' of complex vibrational signals therefore gradually manage to make the very short impulses (Fig. 3) changes with the distance travelled. For example, without causing the plants to perform long, low- short impulses contain both low and high frequency frequency vibrations. We tried many different components, and such signals are transformed into shapes of short electrical signals for the electro- frequency-modulated sweeps of longer duration. magnet and never succeeded in producing short It is interesting that some of the animals do in impulses without a long 'tait' of low-frequency vi- fact produce such impulses. At present, we have bration. As seen in Figs. 3 and 4, the animals' short no evidence that the animals use this information impulses are often followed by a few cycles of low- for locating each other, but in theory they might frequency vibration, but in some cases these vibra- be able to judge the distance and direction to the tions are almost absent. Similarly, the recorded singing animals, if they perform a rough frequency songs did not appear much distorted by reflected analysis of the vibrational signals, and if they are waves. We have no information about the coupling able to process the time intervals between the fre- between animal and plant. 279

One difference between the weak airborne with that reached by Rupprecht (1968) who inves- sounds - which do not seem to play any role in tigated the propagation of drumming signals made the life of these animals (Ichikawa 1976; Gogala by stoneflies living on the plant Phalaris arundina- et al. 1974) - and the vibrational signals is the oc- cea (L.). Rupprecht measured the relevant physical currence of low-frequency vibrations originating parameters of this plant and calculated the propa- from other activities, e.g. movements of wings or gation velocities of the longitudinal (cO and trans- legs (Fig. 3 B). It is possible that these vibrations verse wave (cr). The measured and calculated also carry behavioural information to the other values of % (about 500 m/s) were in good agree- animals. In the bugs and 'small cicadas' studied ment with each other, but the calculated value for here, all the important information is carried by CT (190 m/s) was much larger than the measured means of substrate vibrations. Such signals may value (about 40 m/s). Rupprecht used broad-band also be important in animals which communicate vibrational pulses for his measurements, so the fre- by means of high-frequency airborne sound. For quency is uncertain. We have measured the propa- example, preliminary observations of tettigoniid gation velocity on some stems of Phalaris and can bush crickets have shown that singing animals emit confirm Rupprecht's measured value for frequen- both high- frequency sounds (maximum at cies of about 50 Hz (Table 1). Apparently, Rup- 20-30 kHz) which are not transmitted by the precht measured a bending wave and not a trans- plants - and low-frequency vibrations which are verse wave. As mentioned in the Introduction, transmitted to all parts of the plant. From neu- transverse .waves are not likely to occur in slim rophysiological work there is evidence that the si- rods. Furthermore, Phalaris has an annular cross multaneous presentation of low-frequency vibra- section, and there are no components of motion tion may enhance the response of some central transverse to the surface, neither in transverse neurons to high-frequency sound (Cokl et al. 1977; waves, nor in torsional waves, which can be picked Kfihne et al. 1980). up by a grammophone stylus like that used by Rupprecht. Amplitudes and Wave Types Strategies and Energetics of Communication The amplitudes indicated by the output of the laser vibrometer are velocities in the direction of the Small animals have particular problems in com- laser beam. They may also be expressed as dis- municating with each other. The spatial resolution placements or accelerations (by dividing or multi- of vision varies with the size of the eye (see Land plying with 27~f, wherefis the frequency of vibra- 1981), and small sound emitters are inefficient at tion). The observed accelerations for the bug songs low frequencies. For example, a pulsating, spheri- are between 0.06 and 8 ms -2 in the frequency cal sound emitter with a radius of 2 mm is radiat- range 80-1,500 Hz. These values are much larger ing sound with maximum efficiency only above than those previously reported from measurements 50 kHz (see e.g. Michelsen and Nocke 1974). Some with accelerometers on heavier substrate (Gogala insects do in fact use ultrasound for communica- etal. 1974, measured 10 -3 ms -2 on a wooden tion at distances of several meters, but ultrasonic block about one cm away from the singing animal). signals are not suited for penetrating an environ- The smallest accelerometer available (Brfiel & ment dominated by plants (Michelsen and Larsen, Kja~r 8307) has a weight of 0.3 g. This is equivalent in preparation). The animals studied here are emit- to 10 cm of Thesium stem or to 4 cm of reed stem. ting airborne sounds in addition to the vibrational Earlier measurements of the vibrational songs of songs, but the sound pressure levels are low. At 'small cicadas' on reed or bean stems by means one cm distance from the 'small cicadas' and bugs of this accelerometer showed amplitudes which the sound pressure levels measured are between were about one half of those measured here by 25 and 35 dB (see also Traue 1978a, b; Gogala means of laser light. Obviously, the need for a non- et al. 1974). Assuming a spherical spreading of the loading method is even larger, if one is interested sound (i.e. 6 dB attenuation for each doubling of in light substrates like Thesium stems or dry leaves. the distance to the emitter), these sound levels From the figures for the bug songs indicated above would be sufficient for stimulating even the most one finds that the displacement amplitudes varied sensitive insect ears known only over a few centi- between 8 nm and 4 ~tm, so the songs were well meters (Traue 1978a). The behavioural observa- above the lower limit of the laser vibrometer tions show that the animals do not care about the (about I nm). airborne components of the signals (Gogala et al. The conclusion in this study, that the signals 1974; Strfibing 1977; Ichikawa 1976, 1979). are carried by bending waves, is in disagreement Vibrational signals transmitted through the 280 host plants therefore appear to be a good solution It was further assumed that the animal was to the need for communication over distances up singing on an 'infinite' stem. A more favourable to 1-2 m, if the animals are living on the same position would be at the end of a semi-infinite stem plant. The recording of the vibrational songs dem- (see Cremer et al. 1973). Here Z B is only one onstrate that the animals are able to produce quite quarter of the value indicated in Eq. (6). This large movements normal to the surface of the means that the power required for producing a plants. In the following, we shall attempt a rough vibration of a certain amplitude is only one fourth estimate of the muscular power needed for produc- of that calculated above, or - in other words - ing these signals, using the songs of the bug Sehirus that a certain power input to the stem causes a impressus singing on Thesium stems as an example. two times larger vibration amplitude. This is prob- S, impressus produces broad-band signals, but the ably the reason, why songs are often more intense, main component is at about 500 Hz, where the when the emitting animal sits at the top of the transverse velocity of the plant is about 3" 10 - 4 m/ plant or on a leaf. s. The force (F) needed to produce a bending wave In the Introduction it was mentioned that in a Thesium stem with a transverse velocity (vB) quasi-longitudinal waves in rods show local chan- can be found from ges in rod cross-section associated with the local changes in length. We therefore have to examine vn=F/ZB (5) the possibility that the vibratory motion observed where Z~ is the input impedance of the stem. The normal to the surface of the rods during the propa- exact magnitude of Z B is not known, but the value gation of the vibrational songs is caused by a longi- for the middle of an infinite stem excited by a point tudinal wave. A calculation similar to that per- source is probably not far off(see e.g. Cremer et al. formed above and assuming the emitter to sit at 1973, p. 254) the most favourable position (the end of a semi- infinite stem) demonstrates, however, that longitu- Z~=Zm' cB(1 +j) (6) dinal waves cannot carry the vibrational songs. where m' is the mass per unit length (see Table 1), The input power necessary for causing the ob- cB is the propagation ,(phase) velocity of the served vibration amplitude at 500 Hz is about bending wave, and j is ]/- 1 (a complex input im- 0.3 W, corresponding to 5-10 g of muscle! (The pedance indicates a phase shift between the driving input impedance (Zr) in this case is m" % (Cremer force and the resulting vibration), m' is 3" 10-3 kg/ et al. 1973, p. 249), and R is about 10 -3 for the m and cB is 37 m/s at 500 Hz. So, the numerical stems of Thesium (r = 1 ram), see Eqs. (1) and (2). value of ZB is about 0.3 Ns/m. The fact that these signals are carried by The power input needed for producing the ob- bending waves does not exclude the use of other served wave is FvB which is equal to v2 ZB (cf. kinds of waves in very different kinds of plants. Eq. 5). Inserting the values just estimated, we find Sand transmits both Rayleigh and compressional that the power input needed is about 3.10-s watt. waves, and scorpions use different mechanorecep- The power developed by insect muscles varies with tors for detecting these two kinds of waves (Brow- temperature and other conditions. At 30 ~ it is nell and Farley 1979). We do not know whether often about 70 watt/kg (Jensen 1956), but small insects are also sensitive to vibrations other than insects like the bugs are probably not able to main- those normal to the plant surface. As mentioned tain so high body temperatures. With a power in the Introduction, substrate-borne vibrational output of, for example, 30 watt/kg one needs one signals are known from behavioural observations ~tg of muscle for developing 3.10- s W. The tymbal in several groups of insects, and this kind of com- muscles of the bug have a weight of about 30 gg. munication may appear to be very common. The The animals should therefore have enough muscu- mechanisms involved certainly deserve further lar power available for producing the observed study. waves as bending waves - even if the processes of converting the muscular power to tymbal vibra- tions and of transmitting the tymbal vibrations Acknowledgements. These studies have been generously sup- through the legs to the plant may be rather ineffi- ported by the Danish Natural Science Research Council, the cient. In this calculation it was assumed that the Deutsche Forschungsgemeinschaft, and the Slovenian Research animal only produced energy at 500 Hz, which is Council. We thank A. Bla~evi~ for collecting plants and ani- of course not the case. A ratio of 30:1 between mals, Dr. T. Wraber for determinations of plant species, Dr. J. Toporigi6 and K. Gregersen for providing sonagraphs, and the available and required muscle mass seems ade- Dr. H. Striibing, Dr. O.N. Larsen, Dr. L. Miller and B.B. An- quate for the weaker frequency components as dersen for advice. We also thank an anonymous referee for well. very helpful comments. 281

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