Scale effects and constraints for sound production in katydids (Orthoptera: Tettigoniidae): correlated evolution between morphology and signal parameters

Male katydids (Orthoptera: Tettigoniidae) produce mating calls by rubbing the wings together, using specialized structures in their forewings (stridulatory file, scraper and mirror). A large proportion of species (ca. 66%) reported in the literature produces ultrasonic signals as principal output. Relationships among body size, generator structures and the acoustic parameters carrier frequency (f_c) and pulse duration (p_d), were studied in 58 tropical species that use pure‐tone signals. A comparative analysis, based on the only available katydid phylogeny, shows how changes in sound generator form are related to changes in f_c and p_d. Anatomical changes of the sound generator that might have been selected via f_c and p_d are mirror size, file length and number of file teeth. Selection for structures of the stridulatory apparatus that enhance wing mechanics via file‐teeth and scraper morphology was crucial in the evolution of ultrasonic signals in the family Tettigoniidae.     

Morphological determinants of signal carrier frequency in katydids (Orthoptera): a comparative analysis using biophysical evidence of wing vibration

Male katydids produce mating calls by stridulation using specialized structures on the forewings. The right wing (RW) bears a scraper connected to a drum‐like cell known as the mirror and a left wing (LW) that overlaps the RW and bears a serrated vein on the ventral side, the stridulatory file. Sound is generated with the scraper sweeping across the file, producing vibrations that are amplified by the mirror. Using this sound generator, katydids exploit a range of song carrier frequencies (CF) unsurpassed by any other insect group, with species singing as low as 600 Hz and others as high as 150 kHz. Sound generator size has been shown to scale negatively with CF, but such observations derive from studies based on few species, without phylogenetic control, and/or using only the RW mirror length. We carried out a phylogenetic comparative analysis involving 94 species of katydids to study the relationship between LW and RW components of the sound generator and the CF of the male's mating call, while taking into account body size and phylogenetic relationships. The results showed that CF negatively scaled with all morphological measures, but was most strongly related to components of the sound generation system (file, LW and RW mirrors). Interestingly, the LW mirror (reduced and nonfunctional) predicted CF more accurately than the RW mirror, and body size is not a reliable CF predictor. Mathematical models were verified on known species for predicting CF in species for which sound is unknown (e.g. fossils or museum specimens).     

Distribution of sound pressure around a singing cricket: radiation pattern and asymmetry in the sound field

Male field crickets generate calls to attract distant females through tegminal stridulation: the rubbing together of the overlying right wing which bears a file of cuticular teeth against the underlying left wing which carries a sclerotized scraper. During stridulation, specialized areas of membrane on both wings are set into oscillating vibrations to produce acoustic radiation. The location of females is unknown to the calling males and thus increasing effective signal range in all directions will maximize transmission effectiveness. However, producing an omnidirectional sound field of high sound pressure levels may be problematic due to the mechanical asymmetry found in this sound generation system. Mechanical asymmetry occurs by the right wing coming to partially cover the left wing during the closing stroke phase of stridulation. As such, it is hypothesized that the sound field on the left-wing side of the animal will contain lower sound pressure components than on the right-wing side as a result of this coverage. This hypothesis was tested using a novel method to accurately record a high-resolution, three dimensional mapping of sound pressure levels around restrained Gryllus bimaculatus field crickets singing under pharmacological stimulation. The results indicate that a bilateral asymmetry is present across individuals, with greater amplitude components present in the right-wing side of the animal. Individual variation in sound pressure to either the right- or left-wing side is also observed. However, statistically significant differences in bilateral sound field asymmetry as presented here may not affect signalling in the field.     

The complex stridulatory behavior of the cricket Eneoptera guyanensis Chopard (Orthoptera: Grylloidea: Eneopterinae)

Crickets produce stridulated sounds by rubbing their forewings together. The calling song of the cricket species Eneoptera guyanensis Chopard, 1931 alternates two song sections, at low and high dominant frequencies, corresponding to two distinct sections of the stridulatory file. In the present study we address the complex acoustic behavior of E. guyanensis by integrating information on the peculiar morphology of the stridulatory file, the acoustic analysis of its calling song and the forewing movements during sound production. The results show that even if E. guyanensis matches the normal cricket functioning for syllable production, the stridulation involves two different closing movements, corresponding to two types of syllables, allowing the plectrum to hit alternately each differentiated section of the file. Transition syllables combine high and low frequencies and are emitted by a complete forewing closure over the whole file. The double-teeth section of the stridulatory file may be used as a multiplier for the song frequency because of the morphological multiplication due to the double teeth, but also because of an increase of wing velocity when this file section is used. According to available phylogenetic and acoustic data, this complex stridulation may have evolved in a two-step process.     

Resonating feathers produce courtship song

Male Club-winged Manakins, Machaeropterus deliciosus (Aves: Pipridae), produce a sustained tonal sound with specialized wing feathers. The fundamental frequency of the sound produced in nature is approximately 1500 Hz and is hypothesized to result from excitation of resonance in the feathers'' hypertrophied shafts. We used laser Doppler vibrometry to determine the resonant properties of male Club-winged Manakin''s wing feathers, as well as those of two unspecialized manakin species. The modified wing feathers exhibit a response peak near 1500 Hz, and unusually high Q-values (a measure of resonant tuning) for biological objects (Q up to 27). The unmodified wing feathers of the Club-winged Manakin do not exhibit strong resonant properties when measured in isolation. However, when measured still attached to the modified feathers (nine feathers held adjacent by an intact ligament), they resonate together as a unit near 1500 Hz, and the wing produces a second harmonic of similar or greater amplitude than the fundamental. The feathers of the control species also exhibit resonant peaks around 1500 Hz, but these are significantly weaker, the wing does not resonate as a unit and no harmonics are produced. These results lend critical support to the resonant stridulation hypothesis of sound production in M. deliciosus.     

Unusual abdomino-alary,defensive stridulatory mechanism in the bushcricket Pantecphylus cerambycinus (Orthoptera,Tettigonioidea, Pseudophyllidae)

The bushcricket Pantecphylus cerambycinus has two types of stridulatory mechanisms and acoustical signals. The elytro-elytral mechanism typical for tettigonioid bushcrickets is used to produce a narrow-band calling song (peak frequency 15 kHz). An abdomino-alary mechanism is used for disturbance stridulation. Its stridulatory file is situated on the hind edge of the abdominal tergites and consists of 50-70 parallel ridges, covering the whole width of the tergite. The broad-band sound (peak frequency 10 kHz) is produced by the contact between the file and ribs situated on the upper side of the hindwings which are folded in such a way that their upper side is directed toward the tergites. Defensive stridulation in bushcrickets is reviewed here, and its function and evolution discussed in the context of predator avoidance strategies. © 1996 Wiley-Liss, Inc.     

Characterization and Generation of Male Courtship Song in Cotesia congregata (Hymenoptera: Braconidae)

Background

Male parasitic wasps attract females with a courtship song produced by rapid wing fanning. Songs have been described for several parasitic wasp species; however, beyond association with wing fanning, the mechanism of sound generation has not been examined. We characterized the male courtship song of Cotesia congregata (Hymenoptera: Braconidae) and investigated the biomechanics of sound production.

Methods and Principal Findings

Courtship songs were recorded using high-speed videography (2,000 fps) and audio recordings. The song consists of a long duration amplitude-modulated “buzz” followed by a series of pulsatile higher amplitude “boings,” each decaying into a terminal buzz followed by a short inter-boing pause while wings are stationary. Boings have higher amplitude and lower frequency than buzz components. The lower frequency of the boing sound is due to greater wing displacement. The power spectrum is a harmonic series dominated by wing repetition rate ∼220 Hz, but the sound waveform indicates a higher frequency resonance ∼5 kHz. Sound is not generated by the wings contacting each other, the substrate, or the abdomen. The abdomen is elevated during the first several wing cycles of the boing, but its position is unrelated to sound amplitude. Unlike most sounds generated by volume velocity, the boing is generated at the termination of the wing down stroke when displacement is maximal and wing velocity is zero. Calculation indicates a low Reynolds number of ∼1000.

Conclusions and Significance

Acoustic pressure is proportional to velocity for typical sound sources. Our finding that the boing sound was generated at maximal wing displacement coincident with cessation of wing motion indicates that it is caused by acceleration of the wing tips, consistent with a dipole source. The low Reynolds number requires a high wing flap rate for flight and predisposes wings of small insects for sound production.     

Anatomy of the stridulation apparatus of the beech leaf‐mining weevil and characterization of,and behavioral responses to,stridulation sounds

We investigated auditory signals and morphology of the stridulatory apparatus of the European beech leaf‐mining weevil, Orchestes fagi L. (Coleoptera: Curculionidae), an invasive herbivore now established in Nova Scotia, Canada, to determine their potential for enhancing survey tools to monitor the spread of the species in Canada. We recorded and described sounds produced by adult O. fagi, analyzed the morphology of the stridulatory mechanism for intersexual differences and asymmetry, and examined behavioral responses elicited in conspecifics by playback of stridulation recordings. Adult O. fagi produced sounds under three conditions: male in distress, female in distress, and male in the presence of female. Female distress chirps lasted significantly longer than male distress chirps and male chirps in the presence of females, but peak frequencies and mean number of chirps per s did not differ significantly among the three groups. Morphology of the stridulation structures in male and female O. fagi was compared using scanning electron microscopy. Orchestes fagi have an elytro‐tergal file‐ and scraper‐type sound production apparatus, through which sound is produced upon anterior motion of the abdomen. Female O. fagi have a ‘pars stridens’ that is longer and has more ridges than males. Width and number of ridges per length of pars stridens did not differ between the sexes. Evidence of asymmetry was found in male pars stridens, with the right side being longer than the left. Playback of recorded sounds to adult weevils suggests female O. fagi were repelled by sounds produced by distressed males.     

Relationships between body size and sound‐producing structures in crickets: do large males have large harps?

Abstract. Male crickets produce conspicuous acoustic signals to attract mates and deter potential rivals. These signals are created when a male cricket closes his wings rapidly and a file and scraper mechanism causes several areas of the wing to vibrate. The harp is an area of the wing that is part of the resonating structure. Because the harp acts as part of a mechanical resonator, changes in harp area or mass could influence the frequency of sound produced. Because females exhibit stabilizing selection on the frequency used in male songs, we hypothesized that there would be a negative allometric relationship between body size and harp area. In addition, we examined the degree of asymmetry in the harp, wing, and tibia. We examined this in four different species of cricket: Acheta domesticus, Gryllus bimaculatus, Gryllus rubens , and Teleogryllus oceanicus. For each species, we measured pronotum width as an index of body size, tibia length, and the area of the forewing and harp. There were significant differences among species in their morphological characteristics. We observed consistent directional asymmetry in the harp area but not in the total wing area. When wings did exhibit directional asymmetry, it was in the opposite direction of the directional asymmetry observed in the harp. Within species, larger males typically had larger harps and the relationship between harp area and body size exhibited negative allometry. Wing area exhibited an isometric relationship with body size. Our data provide a potential mechanism linking decreases in song frequency with body size in male crickets, and suggest that sensory constraints might influence the morphology of signaling structures in a similar fashion as genitalia.     

Acoustic studies on the mechanism of sound production in the mating songs of the melon fly,Dacus cucurbitae Coquillett (Diptera: Tephritidae)

The sound production mechanism in the male mating songs for the melon flyDacus cucurbitae Coquillett was acoustically investigated to determine whether sounds resulted from free wing-fanning or stridulation produced by contact between wing and abdominal pecten. Waveforms in the songs of normal (pecten-present) males showed more complex vibrations than those of pecten-removed males. The total harmonic distortion in normal songs was greater than that of the pecten-removed songs. Female (pecten-absent) songs showed different sound signatures on the oscillogram and frequency spectrum from normal male songs. The female songs had more harmonic components than the normal male songs. These results suggest that wing/pecten stridulation of normal male songs produces complicated wing oscillations with a small number of harmonics of near-periodic waveforms and a high harmonic distortion. They also suggest that the free wing-fanning observed during female and pecten-removed male songs produces simple and uniform wing oscillations with many harmonic contents of complex-periodic waveforms and low harmonic distortion. Despite the occurrence of some acoustic differences, pecten-removal did not positively influence the rate of copulation.     

Ultrasound production by genital stridulation in Syntonarcha iriastis (Lepidoptera: Pyralidae): long-distance signalling by male moths?

Males of the pyralid moth, Syntonarcha iriastis Meyrick, perch on vegetation at the tops of trees and bushes and produce ultrasound while their wings are spread and while sclerites at the end of the abdomen are spread to expose the genitalia. Exposing the genitalia appears to engage the sound-producing mechanism; the male genitalia and eighth abdominal sternite of this species are greatly modified and include a file and scraper and possible resonating areas. Sounds produced are consistent between individuals and comprise pulses which are narrow in frequency range, the first pulse being at about 42 kHz and two following pulses at about 57 kHz. The signal is detectable with an ultrasound 'bat' detector from 20 m. Two tettigoniid species (Orthoptera) at the same site produced ultrasonic calls of similar frequencies at the same times as the moth; differences in time-amplitude patterns could be used by orienting moths to recognize conspecifics. Signalling by male S. iriastis is compared with that of other pyralid species in which females are attracted to signalling males. The behaviour of S. iriastis males differs from that of other pyralids in that they do not signal in groups or from a resource attractive to females, and do not possess glands known to produce a 'calling' pheromone. It is suggested, because of these differences, that sound production in this species does not function at close range, as argued for the wax moth Achroia grisella (Fabricius), but instead as a long-distance calling signal.     

Female response song in the ephippigerines Steropleurus stali and Platystolus obvius (Orthoptera,Tettigoniidae)

Stridulation by females of Steropleurus stali and Platystolus obvius in response to the calling song of the males was observed and recorded. The response has only been stimulated by the appropriate male song, either directly or from a recording. The structure of the files and the form of stridulation in both sexes is described. The male song of S. stali is remarkable in that only a few teeth on the file are struck in each wing movement. It is also notable that both opening and closing wing strokes contribute more or less equally to the syllable. The female song is similar but distinct. The song of P. obvius male is a single chirp involving nearly all the teeth on the file and with the main emphasis on the closing syllable. The response song of the female is a very brief chirp. These species are only sporadic singers, but when the female responds they are stimulated into greater activity. They thus contrast with reiterative singers like Ephippiger in which there is no female response. The implications of these contrasting behavioural patterns is discussed.     

A new mechanism of sound production by courting male jumping spiders (Araneae: Salticidae, Saitis michaelseni Simon)

Male Saitis michaelseni Simon (Araneae: Salticidae) produce sounds during courtship which can be heard several metres away. Courting males stridulate on dead leaves and are positioned on the opposite side of the leaf from the female. The courtship display contains both visual and acoustic elements. Courtship consists of three phases. In the first two phases, the male stridulates, and in the third phase, in which he makes tactile contact with the female, he alternates bursts of stridulatory sound with bouts of percussive sound in which the first pair of legs strikes the substratum. Stridulation apparently results from the thickened bases of short hairs on the anterior part of the abdomen moving over two files on the posterior part of the carapace. This stridulatory mechanism has not been previously reported for salticid spiders. The frequency spectra and amplitude modulation patterns of sounds produced by stridulation and percussion are presented.     

Analysis of the Stridulation in Solifuges (Arachnida: Solifugae)

Stridulation in solifuges has not been investigated yet. We performed a comparative analysis of the stridulatory organs and sounds produced by juveniles of various developmental stages and adults (both sexes) of Galeodes caspius subfuscus Birula. The stridulatory organ is of similar morphology in all developmental stages. The sound that they produced was a broad frequency hissing, composed of one or two chirps with maximum at 2.4 kHz. The intensity of the sound was found to increase with body size. Otherwise, no differences were observed between stridulation in juvenile, male and female individuals. Therefore, we suggest that the stridulation in solifuges has primarily a defensive role. As solifuges are neither venomous nor unpalatable, they might imitate an accoustically aposematic organism that shares the same habitat and has similar circadian activity, e.g. vipers. It may also have an intraspecific function in reduction of cannibalistic tendencies.     

Novel use of hair sensilla in acoustic stridulation by New Zealand giant wetas (Orthoptera: Anostostomatidae)

Sound production in New Zealand giant wetas (Orthoptera: Anostostomatidae) includes a femoro-abdominal mechanism, a ticking sound when alarmed (mechanism unknown) and, in two species (Deinacrida rugosa and Deinacrida parva), a tergo-tergal mechanism on the dorsal overlapping surfaces of abdominal tergites. The tergo-tergal mechanism consists of bilaterally paired patches of short curved spines on the dorsal anterior margins of tergites II–V, rubbed by opposing patches of articulated hair sensilla on the underside of each overlapping tergite. The latter are extremely robust, modified mechanoreceptors inserted at an acute angle onto raised bases which greatly restrict movement. They rub sideways against the underlying spines and produce sound during telescopic abdominal contraction which accompanies defence leg kicking stridulation. Movement analysis showed that the abdominal tergites contract asynchronously during stridulation. Sound is produced during both phases of telescoping. Femoro-abdominal sound comprises loud clicks of broadband sound principally below 10 kHz; tergo-tergal sound is a softer hiss spreading broadly from 10 kHz to the ultrasonic above 20 kHz. We propose that the tergo-tergal mechanism may have evolved under predation pressure by the ground gleaning short tailed bat endemic to New Zealand. The use of mechanosensory hair sensilla for sound production is rare in arthropods.     

Mechanical properties of the frog ear: vibration measurements under free- and closed-field acoustic conditions

The acoustically induced motion of the eardrum of the frog was measured by an incoherent optical technique. When free-field sound stimulation was used, the eardrum vibration had a band-pass characteristic with maximum amplitude at 1-2.5 kHz. However, when the sound was presented in a closed-field acoustic coupler the response was low-pass (cut-off frequency about 2.5 kHz). We demonstrate that the motion is the result of the mechanical properties of the eardrum and the sound pressure acting upon it. The net pressure is due to a combination of sound incident directly on the front of the drum and of sound conducted to the rear via internal (resonant) pathways. The frog ear therefore acts as a pressure-gradient receiver at low frequency and a pressure receiver at high frequency. A model is proposed and analysed in terms of its electrical analogue. This model accounts for both our own experimental observations and those of previous studies.     

Intracolony vibroacoustic communication in social insects

Vibrations and sounds, collectively called vibroacoustics, play significant roles in intracolony communication in termites, social wasps, ants, and social bees. Modalities of vibroacoustic signal production include stridulation, gross body movements, wing movements, high-frequency muscle contractions without wing movements, and scraping mandibles or tapping body parts on resonant substrates. Vibroacoustic signals are perceived primarily via Johnston’s organs in the antennae and subgenual organs in the legs. Substrate vibrations predominate as vibroacoustic modalities, with only honey bees having been shown to be able to hear airborne sound. Vibroacoustic messages include alarm, recruitment, colony activation, larval provisioning cues, and food resource assessment. This review describes the modalities and their behavioral contexts rather than electrophysiological aspects, therefore placing emphasis on the adaptive roles of vibroacoustic communication. Although much vibroacoustics research has been done, numerous opportunities exist for continuations and new directions in vibroacoustics research.     

Analysis of Maneuvering Flight of an Insect

Wing motion of a dragonfly in the maneuvering flight, which was measured by Wang et al. was investigated. Equations of motion for a maneuvering flight of an insect were derived. These equations were applied for analyzing the maneuvering flight. Inertial forces and moments acting on a body and wings were estimated by using these equations and the measured motions of the body and the wings. The results indicated the following characteristics of this flight: ( 1 ) The phase difference in flapping motion between the two fore wings and two hind wings, and the phase difference between the flapping motion and the feathering motion of the four wings are equal to those in a steady forward flight with the maximum efficiency. (2)The camber change and the feathering motion were mainly controlled by muscles at the wing bases.     

Coordination of wingbeat and respiration in the Canada goose. I. Passive wing flapping.

The effects of passive wing flapping on respiratory pattern were examined in decerebrate Canada geese. The birds were suspended dorsally with two spine clamps while the extended wings were continuously moved up and down with a device designed to reproduce actual wing flapping. Passive wing motion entrained respiration over limited ranges by both increasing and decreasing the respiratory period relative to rest. All ratios of wingbeat frequency to respiratory frequency seen during free flight (Soc. Neurosci. Abstr. 15: 391, 1989) were produced during passive wing flapping. In addition, the phase relationship between wingbeat frequency and respiratory frequency, inspiration starting near the peak of wing upstroke, was similar to that seen during free flight and was unaffected by perturbations of the wing-flapping cycle. Removal of all afferent activity from the wings did not affect the ability of continuous passive wing movement to entrain respiration. However, feedback from the wings was required to produce rapid within-breath shifts in the respiratory period in response to single wing flaps. In conclusion, although feedback from the chest wall/lung may be more important in producing entrainment during the stable conditions of passive wing flapping, wing-related feedback may be critically involved in mediating the rapid adjustments in respiratory pattern required to maintain coordination between wing and respiratory movements during free flight.