Males of Gryllotalpa australis (Erichson) (Gryllotalpidae) and Teleogryllus commodus (Walter) (Gryllidae) produced their calling songs while confined in respirometers.
G. australis males used oxygen during calling at a mean rate of 4–637ml O2h−1, equivalent to 27·65 mW of metabolic energy, which was 13 times higher than the resting metabolic rate. T. commodus males used oxygen during calling at a rate of 0·728 ml O2 h−1, equivalent to 4·34mW, which was four times the resting metabolic rate.
The sound field during calling by males represents a sound power output of 0·27 mW for G. australis and 1·51×10−3mW for T. commodus.
The efficiency of sound production was 1·05% for males of G. australis and 0·05 % for males of T. commodus. Comparison with other insect species suggests that none is more than a few percent efficient in sound production.
Many insect species produce stereotyped acoustic signals that are important in intraspecific communication. In most species that communicate by sound, the male’s calling song, which seems to attract conspecific females, is the most obvious and the most important component of the repertoire.
Production of the calling song will involve a cost to the producer in the form of an increased use of metabolic energy. The energy required for sound production has been measured for a few insect species (Stevens & Josephson, 1977; Mac Nally & Young, 1981; Prestwich & Walker, 1981). Some part of the energy used during calling is converted into the acoustic energy contained in the call. The efficiency of sound production can be estimated by comparing the amount of energy used during calling with the amount of sound power produced. Few such estimates of the efficiency of sound production in insects have been performed (Counter, 1977; Mac Nally & Young, 1981; K. N. Prestwich, personal communication). It is the aim of this study to measure this efficiency in two grylloid species, the mole cricket Gryllotalpa australis, and the gryllid Teleogryllus commodus.
In grylloids, sound is produced by stridulation. The specialized forewings (tegmina) are opened and closed rapidly with sound being generated on the closing stroke (Michelsen & Nocke, 1974; Bennet-Clark, 1975). A hardened area (the scraper) on the leading edge of one wing contacts a row of sclerotized teeth (the file) on the underside of the opposite forewing. Contact of the scraper with the file teeth generates vibrations that set specialized regions of the forewing into resonant oscillation. Thus, each cycle of wing closing and opening (a wing stroke) generates one pulse of sound. In grylloid insects, the sound produced by a single wing stroke is usually termed a syllable, following Broughton (1963). The wing-stroke rate corresponds to the repetition frequency of syllables in the call.
The two species to be used in this study were chosen because of the differences they exhibit in methods of sound production and in the songs they produce. G. australis, like other mole crickets, produces its call from a specialized burrow (Bennet-Clark, 1970; Ulagaraj, 1976) and the call consists of a continuous train of syllables, i.e. a trill. T. commodus produces its call without the use of a burrow and the call produced is a series of regularly repeated groups of syllables: a chirp is one group of syllables.
MATERIALS AND METHODS
All insects used in these experiments were captured as adults in the field. G. australis males were captured at the Royal Botanic Gardens, Melbourne, when they began to call at dusk. Males were located by homing in upon their calls and were quickly dug from their burrows. T. commodus males were captured by hand at Werribee, 30 km southwest of Melbourne.
All respirometry trials were conducted in the laboratory. The oxygen consumption of calling males of both species was measured manometrically using a constant pressure compensating respirometer after the design of Mac Nally & Young (1981, their fig. 1). In this design two sealed chambers of the same volume are connected by a manometer bore. The experimental animal is placed in one of these chambers (the animal chamber), and as it respires it consumes oxygen and gives out CO2, which is absorbed by a small quantity of NaOH placed in each chamber. Initially the pressure in the two chambers is equal, but as the respired CO2 is absorbed, the pressure in the animal chamber decreases. This is indicated by the movement of a coloured fluid in the manometer bore. A micrometer with attached piston is then advanced to a level which compensates for this pressure difference. The volume of air displaced by the piston provides a measure of the volume of respired oxygen (Davies, 1966).
Two sets of respirometry chambers were used. A larger set of chambers (24×10·5× 11 cm) was used for G. australis. These were filled with 2·0kg of sterile soil rehydrated with 375 ml of distilled water. After addition of the soil the volume of air in the chambers was 1·801. A smaller set of chambers was used for T. commodus. These measured 13×10·5×11 cm and had a volume of 1·251. A piece of cardboard (portion of egg carton) was added to the small chambers to provide cover for the experimental animal.
Respirometry trials on both species followed the same protocol. The experimental animal was released into the animal chamber of the respirometer 24 h before the start of a trial. A Petri dish containing 45 ml of 5 mol l−1 NaOH was placed in each chamber 6 h before the expected time of calling. The chambers were sealed and the complete assembly was transferred to a water bath at 23°C.
Oxygen consumption in G. australis was measured from 5 min after calling began until cessation of calling, usually a period of 20–25 min. For T. commodus, the oxygen consumption of calling males was measured for 15–20 min when the males were calling consistently. Resting rates were measured in the same way during daylight hours, when males of both species were quiescent for long periods. The respirometers were tested regularly for leakages and faults by running trials without a cricket in the animal chamber. All measurements of oxygen consumption were converted to standard temperature and pressure (STP).
Individuals involved in successful respirometry trials were marked and, at a later date, killed and fixed in alcoholic Bouin’s solution. The mesothoracic musculature active during sound production (Bennet-Clark, 1970; Bentley & Kutsch, 1966) was dissected out of the fixed animals, placed in 70% alcohol, rehydrated in saline, blotted dry and weighed.
Measurements of sound output
The sound output of calling males of both species was measured using the following method. A microphone was moved around the calling male or, in the case of G. australis, the entrance to the male’s burrow at a constant distance of 0-2 m. The apparatus was of similar design to that of Mac Nally & Young (1981, their fig. 2), and consisted of a semicircular rod mounted on steel spikes. The rod could be rotated through 180°. The microphone was mounted on this rod with a moveable clamp. By moving the microphone along the rod and by moving the rod itself, a full hemisphere of readings could be obtained.
Readings of sound pressure level were taken at five different angles of elevation: anterior, 45° anterior, dorsal, 45° posterior and posterior. For each of these angles the sound pressure level was sampled at up to four azimuth positions, π/2, 3 π/8, π/4 and π/8, and a lateral reading was taken. The sound field was sampled on only one side of each male (Mac Nally & Young, 1981, their fig. 3).
Sound pressure levels around calling G. australis males were measured using a Bruel & Kjaer Type 4131 microphone connected to a Bruel & Kjaer Type 2203 sound pressure level meter via a 2-m extension lead. Slow root mean square (RMS) levels (time constant Is) were recorded in dB re. 2×l0−5Nm−2. All measurements on G. australis were made in the field. Soil temperatures were between 18 and 20°C. Background noise (all frequencies) was below 65 dB. To check for near-field effects the sound pressure levels of several G. australis males were measured at both 20 and 80cm directly above the burrow mouth.
For T. commodus a Bruel & Kjaer Type 2230 sound pressure level meter was used with a Bruel & Kjaer Type 4155 microphone and a 3-m extension lead. This sound level meter was used in the Leq mode, which records the time-weighted average of a series of fast RMS recordings (time constant 125 ms). This gave a level in dB re. 2×l05Nm−2 which was the equivalent continuous level with the same acoustic energy as the fluctuating (chirped) signal being recorded. A period of 20–30s was found to be sufficient to give a stable level for T. commodus. All the Bruel & Kjaer equipment was calibrated with a Bruel & Kjaer Type 4230 sound level calibrator.
The sound output of T. commodus males was measured in the laboratory, because of the need for partial restraint. Males were placed in small cages of stainless steel mesh (5×5×5 cm; 2mm mesh). Measurements were made when the male called consistently while standing on the floor of the cage. The microphone was moved to the exact position required. The cages were placed on a tray of damp soil 3 cm deep. The temperature was 21·5 ± 1·5°C and background noise in the room was below 60dB.
Additional males of both species were used to measure peak and RMS sound pressure levels 20 cm dorsal to the calling male. The measurements were made with the Bruel & Kjaer Type 2230 sound level meter. Similar measurements were also made on synthesized G. australis calls. Signals were synthesized with the Tektronix FG501 function generator and a homemade synthesizer. They were broadcast through a Phillips Dome Tweeter (AD01610T8) using a Toshiba SB-M30 amplifier. Signals were produced with different duty cycles and measurements were made of the difference between peak and RMS values for the same signal for a range of duty cycles.
Sound production in Gryllotalpa australis
Males of G. australis produce a loud calling song from specialized burrows similar to those constructed by G. vineae (Bennet-Clark, 1970). The calling song of G. australis is a loud trill produced for 20–30 min at dusk on summer nights, when the soil temperature is above 15°C. At 23°C the call has a carrier frequency of 2·54 kHz and a pulse repetition frequency of about 70 Hz.
G. australis males constructed their specialized burrows in the respirometers. Most burrow construction took place in the 2h immediately before the male commenced calling. From 45 respirometry trials, eight successful measurements of oxygen consumption during calling and 11 measurements of oxygen consumption at rest were made. The mean rate of oxygen consumption for calling males was 4·637 ml O2h−1 (S.E. = 0·258). This was an increase of about 13 times the mean resting rate of 0·345 ml O2h−1 (S.E. = 0·017). Mass-specific rates of oxygen consumption were calculated from both total body mass and the mass of muscle involved in sound production. The mean rates for calling males were 5·303 ml O2h−1 gbody mass−1 (S.E. = 0·307) and 117·66 ml O2h−1 g muscle−1 (S.E. = 6·266).
The oxygen consumption rates of resting and calling males were converted to energy equivalents using the oxycalorific conversion factor 19·796 J ml O2−1 at STP (Elliot & Davison, 1975). The energy required for production of the calling song was the total energy used during calling minus the metabolic (resting) rate. For G. australis this was 27·65–2·06 = 25·59mW.
The sound field and power output
Four successful measurements of the sound field were made to the right side of the male’s burrow and four to the left. The sound field was found to be symmetrical around the saggital plane, and so no distinction was made between measurements from the right and left sides. Measurements on six males at 80 cm confirmed that there were no near-field effects associated with measuring at 20 cm from the mouth of the burrow. Differences between the sound pressure levels at the two positions were 11·9±0·3dB, which conforms to the inverse square law.
Means and standard errors of sound pressure levels for each sampling position around calling males are presented in Table 1. These values were used to reconstruct the shape of the sound field around the burrow of a calling G. australis male (Fig. 1). The shape of the sound field in this species is similar to that described for G. vineae (Bennet-Clark, 1970) except that proportionately more of the sound produced is projected posteriorly in G. australis. The differences in the shape of the sound field between these two species may arise from differences in the design of the burrow.
G. australis males construct a burrow which has four openings to the surface, whereas the G. vineae burrow has only two openings.
In G. australis, calling involved the use of 25·59mW of metabolic energy to produce a sound power output of 0·27 mW. Thus, the efficiency of males of this species at converting metabolic to acoustic energy was 0·27/25·59×100 = 1·05 %.
That the measures of sound output used in determining this overall efficiency rating, i.e. slow RMS levels, were true integrations over time of the sound produced was confirmed by measuring both peak and RMS levels on a number of G. australis males and on synthesized G. australis calls. The RMS level of an unmodulated or pure tone is, by definition, half of the peak level, i.e. 3 dB less than the peak level. As the call of G. australis is a pure tone divided into pulses, a true RMS value should be proportional to the ‘on time’ of the pulsed signal, i.e. to the duty cycle. For a duty cycle of 50 %, the RMS level would be half the RMS level for a pure tone of the same amplitude, i.e. 6dB less. This would give an RMS level 9dB below the corresponding peak level. The duty cycle of G. australis males for temperatures between 18 and 25°C varies between 48 and 70% (M. W. Kavanagh & S.-A. Tagney, in preparation). This should give differences between peak and RMS levels of between 9·4 and 6·1 dB. Fig. 2 shows a plot of synthesized G. australis calls with different duty cycles and the difference between peak and RMS levels recorded for these signals. From Fig. 2 duty cycles of 48–70% gave differences between peak and RMS levels of between 9·3 and 6·7 dB, which fits the predictions. Measurements on the calls of G. australis males revealed differences between peak and RMS levels of between 8-0 and 11-1 dB (peak levels; 98·7±l·0dB, N = 15). These differences are slightly higher than predicted, but this is explained by the shape of the pulses in the call of some G. australis males. Some males produce pulses with long attacks and decays, which reduces the effective duty cycle by up to 10–15 %.
Sound production in Teleogryllus commodus
Males of T. commodus produce a complex calling song that contains two types of chirps, as described previously (Leroy, 1966; Hill, Loftus-Hills & Gartside, 1972). For the purposes of the present study, the call of T. commodus at 23 °C is assumed to consist of one complex chirp of five high-amplitude pulses with a repetition frequency of 15 Hz, and 12 smaller pulses at 25 Hz followed by a simple chirp of 12 small pulses, also at 25 Hz. This sequence of two chirps is repeated for the duration of the call at a rate of 30 min−1. The carrier frequency of the call is 3·8 kHz at 23 °C (Hill, 1974).
From 35 respirometry trials, eight successful measurements of oxygen consumption during calling were obtained. Eleven measurements of oxygen consumption for resting males were also made. The mean rate of oxygen consumption in calling males was 0·728 ml O2h−1 (S.E. =0·048). This was nearly four times the resting rate of 0·187 ml O2h−1 (S.E. = 0·12). Mass-specific rates were calculated as for G. australis. For calling males the mass-specific rates were 1·209 ml O2h−1 g body mass−1 (S.E. = 0·048) and 76·652mlO2h−1gmuscle−1 (S.E. = 3·949). The energy used during sound production by T. commodus was calculated by using the same method as for G. australis and yielded a value of 3·22mW.
Three successful measurements of the sound field were made to the right of a male and two to the left. The sound field was found to be symmetrical. Table 2 shows the means and ranges of sound pressure levels around calling T. commodus males. A reconstruction of the sound field was not attempted due to the low number of SPL measurements obtained for this more mobile species. The sound power output of T. commodus was calculated as for G. australis. The mean sound power output was l·51×10−3mW (S.E. = 2·5× 10·4). Therefore, T. commodus males are 1·51×10−3/ 3·22×100 = 0·05 % efficient at converting metabolic to acoustic energy.
Measurements of peak and RMS levels on T. commodus males revealed that, as with G. australis the RMS levels used were good measures of the average sound output. Peak levels for T. commodus males were 8·8–11·5 dB above the fast RMS levels (peak levels, x̄ = 83·3 ± 1·1 dB, N = 14). However, in the case of T. commodus, which produces a chirped call, a series of these fast RMS levels was averaged over a longer period to give a level for the call as a whole. These Leq values were used in all calculations.
The cost of sound production
Sound production in males of G. australis and T. commodus incurs a considerable cost in the form of increased metabolic expenditure. Table 3 compares the increases in oxygen consumption rate observed in these two species with those found in other species of sound-producing insect. All the other species in Table 3 produce trilled calls. As noted earlier, G. australis produces a trilled call, and its mass-specific oxygen consumption rate is consistent with the comparatively high rates recorded from the other trilling species. T. commodus produces a chirped call, and shows a comparatively low rate of oxygen consumption during calling.
The cost of sound production depends on many inter-related factors, the most accessible of which is the wing-stroke rate (Prestwich & Walker, 1981). A high wing-stroke rate requires a greater amount of metabolic energy, and so variation in wingstroke rate may explain some of the variation in oxygen consumption rates for the species in Table 3. Oxygen consumption rates per wing stroke for the same group of sound-producing insects are displayed in Table 4. For the trilling species, the rate of oxygen consumption per wing stroke is calculated using the formula from Prestwich & Walker (1981):
The cost of calling expressed as oxygen consumption per wing stroke is similar for several species when the calculations are based on rates of oxygen consumption per gram body mass (Table 4). However, these similarities disappear when the mass of sound-producing muscle is used. As the total body mass includes many structures not directly responsible for sound production (e.g. reproductive structures), this may not be as reliable a measure as the mass of sound-producing muscle. Therefore, there is still a degree of variation in the cost of sound production that is not directly dependent on the wing-stroke rate. This variation may arise from several sources, such as differences in the structure of the file teeth (density, depth, rigidity and pitch), which will affect the amount of force that must be produced to overcome the resistance of these teeth (Prestwich & Walker, 1981).
While there is variation in the cost of sound production between insect species, all the recorded values fall within a fairly narrow range. The range of oxygen consumpion rates per wing stroke for sound-producing insect species overlaps with the range of oxygen consumption rates per wing beat for flying insects (Stevens & Josephson, 1977).
The efficiency of sound production
Neither G. australis nor T. commodus males are efficient at converting metabolic energy used during calling into sound output (1·05% and 0·05% efficient, respectively). There are only two other direct measures of the efficiency of sound production in insects available to compare with the results obtained here. Mac Nally & Young (1981) calculated an efficiency of 0·82% for the bladder cicada, Cystosoma saundersti while K. N. Prestwich (personal communication) has calculated a value of 0·23 % for the gryllid Anurogryllus arboreus. The similarity of these values indicates that sound production is an inefficient process in the species of insects studied so far.
While there are no further direct measures of efficiency in insects, Bennet-Clark (1970) has estimated the efficiency of the conversion of mechanical energy generated by sound-producing muscle to sound power output for two species of mole crickets. Since Bennet-Clark (1970) gives the wing-stroke rates (i.e. pulse repetition frequencies) and the masses of the sound-producing muscles (i.e. wing closers and openers) for G. vineae and G. gryllotalpa, we can estimate the probable energetic cost of calling in these two species if we assume that they use oxygen during calling at the same rate per wing stroke per gram muscle as does G. australis. Using these figures it is estimated that the amount of energy used by G. vineae during calling is 37·94 mW. A resting rate can be derived from the resting rate per gram muscle found for G. australis and correcting for the muscle mass of G. vineae. This gives a resting rate for G. vineae equivalent to 2·72 mW. Thus, the increase in metabolic energy used during calling by G. vineae is estimated to be about 35·22 mW. As Bennet-Clark (1970) has measured the sound output in these two species, we can also estimate the overall efficiency of calling in G. vineae and G. gryllotalpa. The sound power output of G. vineae is 1·2 mW (Bennet-Clark, 1970) and thus the efficiency of this species is probably about 1·2/35·22×100 = 3·41 %. Similar calculations for G. gryllotalpa give an efficiency of 0·5 %. If these calculations are based on oxygen consumption rates of G. australis per gram body mass, rather than per gram muscle mass, the values obtained are 1·36 % efficiency for G. vineae and 0·06 % for G. gryllotalpa. Mac Nally & Young (1981) have also estimated an overall efficiency for G. vineae by a different method, arriving at a value of 5 %.
These estimates for G. vineae and G. gryllotalpa illustrate two points when compared with the calculated efficiency of G. australis. First, even in the most efficient of these species, G. vineae, the efficiency of converting metabolic to acoustic energy is still low. Second, there are quite large differences in the efficiencies of closely related species.
The efficiency of sound production calculated for G. australis and those estimated for G. vineae and G. gryllotalpa are higher than those calculated for the gryllids T. commodus and A. arboreus. The gryllid values are also lower than the 0-82% calculated for the cicada C. saundersii. As already mentioned, the efficiency of sound production in mole crickets is improved by the use of specialized burrows.
C. saundersii employs a similar strategy. A large, air-filled cavity in the abdomen acts as a large resonant sound radiator which improves sound radiation and, hence, overall efficiency (Mac Nally & Young, 1981; Alexander, 1983). T. commodus and A. arboreus use no such devices to improve the effectiveness of sound radiation and thus, in this respect, would be expected to be less efficient producers of sound.
The measurements of efficiency calculated for G. australis and T. commodus males may be slight underestimates of the true value due to some absorption of the sound output by the substrate. However, in the case of the mole cricket, the shape and function of the burrow makes it unlikely that much sound is lost to the soil or down the burrow (Bennet-Clark, 1970). T. commodus males do not have the benefit of a burrow to direct their sound output, so it is possible that some of the sound output was absorbed by the soil. However, even if only half the sound output was measured, which seems very unlikely, the overall efficiency of converting metabolic to acoustic energy would still be only 0·18%. This inflated value remains much less than those for G. australis (this paper) or C. saundersii (Mac Nally & Young, 1981).
It should be noted that these estimates of the efficiency of sound production obtained for G. australis and T. commodus are confined to energy transfer during the brief periods when the animals are actually calling. Obviously additional factors would need to be taken into account to estimate the cost of calling as a fraction of the animals’ total energy budget. In particular, the construction of a burrow by males of G. australis is likely to be an energetically expensive activity, which would add to the cost of sound production. Although T. commodus does not expend energy on constructing a burrow, it does call for much longer periods than G. australis and this would add to the cost of sound production. Hence it might turn out that sound production involves a similar proportion of the total energy budget in these two species in spite of their different calling strategies.
I wish to thank Drs David Young, Ralph Mac Nally and Jane Doolan for their help and for critically reading this manuscript, also Dr Murray Littlejohn and Bill Hopper for helpful discussions on sound measurement. My thanks go to the management and staff of the Royal Botanic Gardens, Melbourne. Financial support for this work was provided by a grant to Dr David Young from the Faculty of Science, University of Melbourne. The author was in receipt of a Commonwealth Postgraduate Research Award.