Entomological Review, Vol. 80, No. 9, 2000, pp. 1157-1169. Translated from Zoologicheskii Zhumal, Vol. 79, No. 10, 2000. Original Russian Text Copyright © 2000 by Lapshin, Vorontsov. English Translation Copyright © 2000 by MAIK "Naulca /Interperiodica" (Russia). Ultrasonic Emission by Noctuid Moths (Lepidoptera, Noctuidae): Main Characteristics of Signals and Possible Mechanisms of Their Generation D. N. Lapshin1 and D. D. Vorontsov2 JInstitute for Problems of Information Transmission, Russian Academy of Sciences, Moscow, 127994 Russia 2Institute of Developmental Biology, Russian Academy of Sciences, Moscow, 117808 Russia Received November 19,1999 Abstract—Morphological and acoustic studies of the sound-producing mechanism in noctuid moths were carried out on Amphipyra perflua. Two laterally symmetrical pairs of complementary areas adjacent to each other are responsible for generation of ultrasonic bursts. One pair is located on the ventral surface of the fore-wing base, and the other, on the metascutum. The surface of these areas is covered with inclined cone-like structures 18-25 µm high. The density of cones is as high as 3 per 100 µm2. The aculeae of both the complementary areas are oriented toward each other and can serve to couple the wings to scutum. When uncoupling, these structures produce an ultrasonic pulse. Moths with removed wing coupling areas cannot emit clicks. Noctuid moths produce ultrasonic clicks during flight. The peak amplitude of these clicks varies between 79 and 84 dB SPL at a distance of 5 cm from a moth, with their mean duration being 67 µs. The clicks have a broad-band (> 100 kHz) spectrum with the main peaks, at 57 and 78 kHz. Artificially generated clicks have a similar spectrum. The regular pattern of emission with one click per second or every third wing-beat was often observed in the nature and in conditions of tethered flight. The adaptive importance of the acoustic behavior of moths is discussed. Noctuid moths are known to emit ultrasonic bursts in nism, proposed by Agee. It should be mentioned that short flight. This phenomenon was first discovered by Roeder and ultrasonic pulses do appear at the upper point in mutual Treat (1957). According to Kay (1969), signals of the contact of the hind wings of a flying moth (Waters and noctuid moth Heliothis zea have the form of rapidly damped Jones, 1994), but their amplitude, as a rule, does not exceed paired clicks with filling frequency of 50 kHz and duration 65 dB SPL, which is at least 10 dB (20 dB on the average) of 180 us each. The pulses in a pair are separated by 190 µs. less than the amplitude of clicks recorded by Kay and Agee. The sound intensity is 98.6 dB SPL at a distance of 1.5 cm In the paper by Zhantiev et al. (1993), the basic types of noctuid signals and examples of their spectra were given. from the source. Kay assumed that the acoustic pulse gen- The free-flying moths were demonstrated to produce ultra- erator is of the tymbal type and, by analogy with arctiid sound too, i.e. the acoustic emission of noctuids cannot be moths (Arctiidae), is located on the metepisterna. However, accounted for by insect fixation in experimental conditions. this assumption has not been verified experimentally so far. Parameters of the recorded signals were independent of Relying on stroboscope observations of flying noctuid species, sex, and age of moths. moths, Agee (1971) concluded that acoustic pulses may Several noctuid moth species are known, hypothetically either arise from the wing flapping at the upper point or be using the acoustic signals for intraspecific communication: an experimental error resulting from the contact of wings Thecophora fovea employs the stridulation mechanism of with the mounting holder. In 1993, Agee's conclusions were emission (Surlykke and Gogala, 1986); Amyna natalis, the revised in view of new data. Using the technique of moth tymbal mechanism on the wings (Heller and Achmann, photographing at the moments of click recording, Zhantiev 1993); and Pseudoips fagana, the tymbal mechanism on the et al. (1993) demonstrated that, in noctuid moths, the abdominal segment (Skals et at., 1996). However, only position of wings in emission is close to horizontal. This fact males emit sounds in all the examples. In all three cases, the is contradictory to the model of the generation mecha- intensity of the acoustic signals is 1-2 orders of magni- 1157 1158 LAPSHIN, VORONTSOV tude higher than the values recorded by Kay and by Zhantiev by noctuids—amplitude, duration, spectrum and dynamics of et al. Up to now, the search for a more general mechanism of the click sequence; (2) investigate the possibility of generation of the sound emission for noctuid moths has not been ultrasonic signals by the areas of the wing-thorax coupling successful. and by the cuticular structures on the body of noctuids In many nocturnal moths, including noctuid moths, the (including metepisterna); and (3) carry out a comparative fore wing in the resting position is coupled with the body by analysis of the acoustic parameters of both natural and means of complementary areas covered with cone-shaped artificial clicks. processes—microtrichia (Kuijten, 1974). The first area is located on the posterior margin of the hind wing, and the MATERIALS AND METHODS second one lies on the metascutum surface. Both males and females possess such structures. When these areas are For the most part, experiments was carried out with uncoupled artificially (manually), a loud click is distinctly Amphipyra perflua F. These noctuid moths of both sexes heard. Presumably, the moths generate ultrasound by this were trapped using a food attractant (fermented mixture of mechanism. beer and honey) in Moscow and environs in July-August 1996-1999. A total of 50 specimens of this species were Roeder and Treat (1957) assumed that noctuids survey the used in the experiments. surrounding space by emitting clicks. The possibility of echolocation in moths was discussed in different aspects by In addition, 12 specimens of the noctuid moth Hydraecia all those who studied the emission of clicks. In the recent micacea Esp. captured at light of a fluorescent lamp were decade, data confirming this hypothesis have been obtained tested for capability of acoustic emission. (Lapshin et al., 1993; Lapshin, 1995; Lapshin and Vorontsov, The experiments were performed in the evening and at 1998). Thus, the biological function of the signals under night in laboratory at a temperature of 18-20°C. study became more definite. In this connection, the problem of identification of the mechanism of the ultrasonic burst A Study of Spectral Characteristics of Moths' Clicks emission has assumed special importance. An insect was pasted with warm wax to a thin wire, so It can be seen from the oscillogram of a series of bursts, that the wings did not touch the bracing in flapping. To presented in the paper by Roeder and Treat (1957), that the record acoustic signals, a RFT 301 (1/4") microphone was experimental moth produced clicks at every wing-beat. placed at a distance of 5 cm from the moth, in front of it and Similar examples were also given in other reports (Agee, above its longitudinal axis. The electric signal from the 1971; Zhantiev et al., 1993). However, the latest microphone output was amplified (microphone amplifier investigations showed that in some cases the emission rate of RFT 00023), passed through high-pass filtering (cutoff "one click per each wing-beat" is not obligatory and even not frequency 1 kHz), and fed into the input of a Hewlett the basic (Lapshin, 1996). It was found that, when presented Packard HP54601B digital storage oscilloscope. The with visual stimuli, the noctuid moth Amphipyra perflua sampling frequency of the built-in analog-to-digital converter of tends to emit with an interval 3Tb between the clicks (Tb the the oscilloscope is 1.25 MHz, which corresponds to a wing-beat period, approximately 30 ms). quantization interval of 0.8 µs. From the oscilloscope output From the standpoint of the echolocation system efficiency, the digital data were delivered to a computer by means of the the interpulse time of the probing signals is one of the basic RS-232 interface. parameters determining the rate at which the information is The subsequent processing of the results included updated. In this connection, it was necessary to investigate in normalization of click oscillograms to the maximum amplitude, more detail the dynamics of the spontaneous acoustic emission alignment of the base line slope, measuring the duration of by noctuids in addition to the studies in which the dependence signals, and calculation of their spectra, The duration of a of the click emission frequency on visual or echolocation separate impulse was conditionally taken equal to the total information was revealed (Lapshin, 1996; Lapshin and length of an integer number of component half-waves with Vorontsov, 1998). amplitude of no less than 0.2 of the maximum value. The The purposes of this study were as follows: (1) to spectra were calculated by the method of sequential analysis determine the characteristics of the acoustic emission of an inscribed piecewise linear function in the fre- ENTOMOLOGICAL REVIEW Vol. 80 No. 9 2000 ULTRASONIC EMISSION BY NOCTUID MOTHS 1159 quency range 1-100 kHz with a step of 1 kHz (D'yakonov, Another part of insects of the second set (10 specimens) 1987). Original specially designed computer programs were was used in experiments in which the coupling areas were used to solve particular problems of this study. studied as sound generating structures. A moth narcotized with chloroform was placed under the microphone, and Measurement of Click Amplitude acoustic impulses were produced by moving manually the distal part of the fore wing.