SOUND PRODUCTION IN THE LARVAE OF GEOTRUPES SPINIGER (MARSHAM) (COLEOPTERA: GEOTRUPIDAE)

ABSTRACT

This paper focuses on sound production in the larvae of Geotrupes spiniger (Marsham) (Coleoptera: Geotrupidae). A single stridulatory apparatus was identified and then analysed from a structural point of view. Sound was studied using spectography and results included a quantitative analysis with characterizing physical parameters. Results highlight the need to study stridulation in Geotrupidae more in detail, to improve our understanding of its evolutionary and biological meaning.     

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.     

Colony Wide Behavioral Contexts of Stridulation in Imported Fire Ants (Solenopsis invicta Buren)

Red imported fire ants, Solenopsis invicta, possess stridulatory organs and stridulate in a variety of contexts. We used a stethoscope mounted microphone to study stridulation at the colony level in the context of emigration, disturbance, and excavation. In conjunction with preliminary observations of nest and foraging activities, our results suggest stridulation serves multiple functions in S. invicta. Stridulation was not significantly increased in colonies during responses to disturbance, and only marginally during colony emigration. Colonies involved in excavation, however, exhibited a significant increase in stridulatory activity. Four possible explanations for the function of stridulation in this context are discussed in relation to the stridulatory behavior of individuals, solitary wasps, and published literature on formicid stridulation.     

Auditory information processing in stridulating grasshoppers: tympanic membrane vibrations and neurophysiology

During stridulation in the gomphocerine grasshopper Omocestus viridulus the leg movements, sound pattern and either summed auditory nerve activity or single interneuron activity were recorded. Simultaneous laser interferometric and vibrometric measurements of the displacement and velocity of the tympanic membrane were performed at the pyriform vesicle (d-receptor group). Slow displacements of the tympanic membrane occur in phase with the ventilatory and stridulatory rhythm and reach 10 m_peak-peak and 1–3 m_peak-peak in amplitude, respectively. Additionally, the tympanic membrane oscillates maximally in the range 5–10 kHz. These high-frequency oscillations are due to sound production and motor activity and correspond in amplitude to oscillations evoked by sound pressures of 90-dB SPL. They activate the auditory receptors during most of the stridulatory cycle even during mute stridulation. Only at the lower reversal point of the leg movement are membrane vibrations and receptor activity at a minimum. As a consequence the response of receptors and interneurons to auditory stimuli are generally impaired and an auditory response of receptors and interneurons can be elicited only during a short period at the lower reversal point. Although in this phase of the stridulatory cycle auditory sensitivity is present, males do not show phonotactic responses towards female songs during ongoing own stridulation.     

Pharmacological Activation of Stridulation in the Grasshopper Chorthippus albomarginatus (Orthoptera: Gomphocerinae)

Calling and courtship stridulatory behavior of Chorthippus albomarginatus was induced by injections of acetylcholine agonists into the protocerebrum. Pharmacologically induced stridulation, in many parameters, was quite similar to the natural behavior. However, the order of the courtship element alternation was different from that of the natural song. In some cases the pharmacologically induced stridulation included only one or two courtship elements. Based on the exclusive stimulation of a particular element of courtship songs and similarity of its movement pattern with the calling song, both patterns of Ch. albomarginatus stridulation appear to be homologous. The results obtained on this species confirm the idea of a hierarchic organization of the central nervous control of stridulation in gomphocerine grasshoppers and indicate participation of certain protocerebrum structures in this control.     

EVIDENCE FOR A HYDRODYNAMIC MECHANISM OF SOUND PRODUCTION BY COURTING MALES OF THE NOTCHTONGUE GOBY,BATHYGOBIUS CURACAO (METZELAAR)

ABSTRACT

Male gobies of the genus Bathygobius are soniferous during courtship. The mechanism by which the sounds are produced is, however, unknown. Early studies on sound production by males of B. soporator suggested that these sounds are hydrodynamic in nature, being produced by the forcible ejection of water through the gill opening. The mechanism of sound production by the closely related species B. curacao was investigated and three lines of evidence are presented which support the hydrodynamic hypothesis. First, similarities between the sounds produced by courting males and by ejecting water through a pipette demonstrated that hydrodynamic forces can readily produce such sounds. Second, the behavioural motor patterns occurring during sound production are consistent with the hypothesis that water is being ejected through the gill openings. Finally, morphological examination revealed an apparent lack of specialised features associated with sound production, effectively eliminating stridulatory and swim bladder mechanisms. These results represent the strongest evidence to date in support of any proposed mechanism of sound production in the gobiids.     

Consistency of females’ stridulatory behaviour during inter‐sexual interactions in spiders

In a sexual context, it is expected that females base their choice of mate on the behaviours that males perform during courtship, as such behaviours are associated with the male's mate quality. Stridulation is one form of female communication in arthropods, for example, spiders. In spiders, stridulation during sexual interactions is relatively common in some groups but mainly restricted to males. In the pholcid spider Holocnemus pluchei (Pholcidae), both sexes have stridulatory organs. The aims of the present work were to: (a) determine possible differences in the frequency of occurrence of stridulation between females during inter‐sexual interactions, (b) establish female consistency in stridulation along repeated interactions and (c) analyse if female stridulation is associated with certain male behaviours during pre‐copulatory courtship and with male size. Female H. pluchei showed highly repeatable differences in their frequency of stridulation across consecutive encounters with males (ICC = 0.64). However, only a modest level of repeatability was detected in total time females spent stridulating across trials (ICC = 0.19). Females’ mean stridulatory behaviour did not change across ten consecutive trials spread across 20 days, and their behaviour was apparently unaffected by male persistence of copulatory attempted and/or size. These results imply that the frequency of female stridulatory behaviour is a trait that is highly characteristic of each individual. Finally, our work opens the door to determine whether behavioural consistency manifests in other ecological contexts and their functional implications.     

Reverse stridulatory wing motion produces highly resonant calls in a neotropical katydid (Orthoptera: Tettigoniidae: Pseudophyllinae)

This paper describes the biomechanics of an unusual form of wing stridulation in katydids, termed here 'reverse stridulation'. Male crickets and katydids produced sound to attract females by rubbing their forewings together. One of the wings bears a vein ventrally modified with teeth (a file), while the other harbours a scraper on its anal edge. The wings open and close in rhythmic cycles, but sound is usually produced during the closing phase as the scraper moves along the file. Scraper-tooth strikes create vibrations that are subsequently amplified by wing cells specialised in sound radiation. The sound produced is either resonant (pure tone) or non-resonant (broadband); these two forms vary across species, but resonant requires complex wing mechanics. Using a sensitive optical diode and high-speed video to examine wing motion, and Laser Doppler Vibrometry (LDV) to study wing resonances, I describe the mechanics of stridulation used by males of the neotropical katydid Ischnomela gracilis (Pseudophyllinae). Males sing with a pure tone at ca.15 kHz and, in contrast to most Ensifera using wing stridulation, produce sound during the opening phase of the wings. The stridulatory file exhibits evident adaptations for such reverse scraper motion. LDV recordings show that the wing cells resonate sharply at ca. 15 kHz. Recordings of wing motion suggest that during the opening phase, the scraper strikes nearly 15,000 teeth/s. Therefore, the song of this species is produced by resonance. The implications of such adaptations (reverse motion, file morphology, and wing resonance) are 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.     

COMPARATIVE ANALYSIS OF SWIMBLADDER (DRUMMING) AND PECTORAL (STRIDULATION) SOUNDS IN THREE FAMILIES OF CATFISHES

ABSTRACT

Among teleosts, only representatives of several tropical catfish families have evolved two sonic organs: pectoral spines for stridulation and swimbladder drumming muscles. Pectoral mechanisms differ in relative size between pimelodids, mochokids and doradids, whereas swimbladder mechanisms exhibit differences in origin and insertion of extrinsic muscles. Differences in vocalization among families were investigated by comparing distress calls in air and underwater. High frequency broad-band pulsed sounds of similar duration were emitted during abduction of pectoral spines in all three families. Adduction sounds were similar to abduction signals in doradids, shorter and of lower sound pressure in mochokids, and totally lacking in pimelodids. Simultaneously or successively with pectoral sounds, low frequency harmonic drumming sounds were produced by representatives of two families. Drumming sounds were of similar intensity as stridulatory sounds in pimelodids, fainter in doradids, and not present in mochokids. Swimbladder sounds were frequency modulated and the fundamental frequency was similar in pimelodids and doradids. The ratio of stridulatory to drumming sound amplitude was higher in air than underwater in both doradids and one of the pimelodids. Also, overall duration of pectoral sounds, compared to swimbladder sounds, was longer in air than underwater in one doradid and pimelodid species. This first comparison of vocalization within one major teleost order demonstrates a wide variation in occurrence, duration, intensity and spectral content of sounds and indicates family- and species-specific as well as context- (receiver-) dependent patterns of vocalization.     

A unique form of light reflector and the evolution of signalling in Ovalipes (Crustacea: Decapoda: Portunidae)

The first demonstration, to our knowledge, of an evolutionary shift in communication mode in animals is presented. Some species of Ovalipes display spectacular iridescence resulting from multilayer reflectors in the cuticle. This reflector is unique in animals because each layer is corrugated and slightly out of phase with adjacent layers. Solid layers are separated from fluid layers in the reflector by side branches acting as support struts. An effect of this reflector is that blue light is reflected over a ''broad'' angle around a plane parallel to the sea floor when the host crab is resting. Species of Ovalipes all possess stridulatory structures. The shallow-water species with the best developed stridulatory structures are non-iridescent and use sound as a signal. Deep-water species possess poorly developed stridulatory structures and display iridescence from most regions of the body. In deep water, where incident light is blue, light display is highly directional in contrast to sound produced via stridulation. Sound and light display probably perform the same function of sexual signalling in Ovalipes, although the directional signal is less likely to attract predators. Deep-water species of Ovalipes appear to have evolved towards using light in conspecific signalling. This change from using sound to using light reflects the change in habitat light properties, perhaps the hunting mechanisms of cohabitees, and its progression is an indicator of phylogeny. The changes in sexual signalling mechanisms, following spatial–geographical isolation, may have promoted speciation in Ovalipes.     

Stridulatory pattern generation in acridid grasshoppers: metathoracic interneurons in Stenobothrus rubicundus (Germar 1817)

Stridulation was elicited in tethered gomphocerine grasshoppers of the species Stenobothrus rubicundus in order to identify interneurons of the stridulation pattern generator, and describe their morphological and physiological properties. Nine types of such neurons could be found and characterized; eight of those could additionally be compared to corresponding neuron types previously known from other species. As shown in detail for one selected type, the neurons of the stridulation pattern generator are very similar in their anatomical appearance, and possess similar physiological qualities at least in two species with similar stridulation patterns. Stridulation interneurons of species with largely different stridulatory motor patterns have a similar morphology, but show a different activation timing throughout the stridulation. Nevertheless, special properties such as resetting or initiation capability of certain stridulation interneurons seem to be conserved throughout the species. The results suggest that the stridulation pattern generator of different species consists of a uniform set of interneurons that change their activity pattern to produce species-specific song movements.     

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.     

‘Switching-off’ of an auditory interneuron during stridulation in the acridid grasshopperChorthippus biguttulus L.

Summary In freely moving grasshoppers of the speciesChorthippus biguttulus compound potentials were recorded from the neck connectives with chronically implanted hook electrodes. The spikes of one large auditory interneuron, known as the G-neuron (Kalmring 1975a, b) were clearly distinguishable in the recordings and the neuron was identified by its physiology and morphology. In quiescent grasshoppers the G-neuron responds to auditory and vibratory stimuli, but responses to both stimuli are suppressed during stridulation in males (Fig. 1, top, Fig. 7). When a male's wings were removed so that the stridulatory movements of its hindlegs produced no sound, the suppression of the G-neuron response still occurred (Fig. 1, bottom). When proprioceptive feedback from the hindlegs was reduced, by forced autotomy of the legs, the switching-off remained incomplete (Fig. 3) (production of stridulatory patterns was inferred on the basis of electromyograms from the relevant thoracic musculature). Imposed movement of the hindlegs, on the other hand, suppressed the G-neuron response in a graded fashion, depending on the frequency of the movement (Figs. 4 and 5). These experiments suggest that the switching-off is brought about by a combination of proprioceptive feedback and central efferences. The switching-off phenomenon could either protect the grasshopper's auditory pathway from undesired effects of overloading by its own intense song (e.g. self-induced habituation as described by Krasne and Wine 1977) and should therefore apply for most auditory neurons. Alternatively it could prevent escape reflexes from being triggered by stridulatory self-stimulation and consequently might apply only for neurons involved in such networks (as the G-neuron might be).     

Stridulatory behaviour in a New Zealand weta, Hemideina crassidens

Using a femoral-abdominal stridulatory mechanism, wetas produce the following stridulatory behaviours: aggression, mating, calling, defence and disturbance. Syllable period, rather than number of syllables/echeme or syllable duration, was the most stereotyped temporal parameter for aggression, mating and calling stridulation. Coefficients of variation of the above parameters were large and overlapped considerably for aggression and mating stridulation. We concluded that, for these two behaviours, a basic sound pattern is used to convey different messages to female and male receiver wetas, respectively, but the syllable period of the pattern decreases with increased excitation of males in aggressive encounters. In adult male combat, winners stridulated last in a bout, and produced significantly more aggression sounds than losers.     

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).     

Circadian control of spermatophore formation in the cricket Teleogryllus commodus Walker

The cricket Teleogryllus commodus has a circadian rhythm in spermatophore formation. A spermatophore is present 1–5 hr before the onset of stridulation under LL, DD and LD 12 : 12; it is retained during the whole stridulatory phase and disposed of within a variable time after termination of singing. Overwhelmingly one spermatophore is produced during a 24 hr-period. Severance of the abdominal nerve cord or removal of the accessory glands prevent spermatophore formation, but does not inhibit periodical stridulation; when a spermatophore is removed from a singing male, stridulation continues after a short time. Coagulation of the pars intercerebralis stops spermatophore production and singing; severance of the optic lobes rends both processes arhythmical. The rôle of the pars intercerebralis as an intermediary link between the timing-device and the effector organs is discussed.     

Neuropharmacological evidence for inhibitory cephalic control mechanisms of stridulatory behaviour in grasshoppers

In gomphocerine grasshoppers the neuromuscular patterns of stridulatory hindleg movements are produced by metathoracic rhythm generators under the control of cephalic command neurons. Injections of cholinergic agonists into the protocerebrum activate this command system which induces the performance of stridulatory sequences, resembling natural species specific movements. Injections of GABA, glycine and picrotoxin into the central protocerebrum of the species Omocestus viridulus, Chorthippus mollis and Ch. biguttulus revealed a contribution of inhibitory mechanisms to the control of the stridulatory behaviour. The experiments suggest that inhibition interferes with the cephalic command systems at three levels: (1) sustained inhibition through picrotoxin sensitive receptors acting on all command units while grasshoppers are at rest, and during stridulation on all command units except the one activating the pattern generators of the currently performed movements; (2) premature termination of song sequences, experimentally induced by injections of GABA and glycine; and (3) coupling of a timing mechanism that terminates a song sequence or its subunits with a particular movement pattern after specific durations. These results together with those from previous studies on the pharmacological activation of stridulatory behaviour suggest that a balance of inhibitory and excitatory inputs to the command system selects the appropriate song type and controls its performance. Accepted: 11 June 1998     

Pharmacological brain stimulation releases elaborate stridulatory behaviour in gomphocerine grasshoppers – conclusions for the organization of the central nervous control

Grasshoppers produce a variety of sounds generated by complex movements of the hindlegs. Stridulation, performed in the context of partner finding, mating and rivalry, can be released by pressure injection of cholinergic agonists into the protocerebrum. Particularly stimulation with muscarinic agonists induced long-lasting stridulation that resembled the natural behaviour to an astonishing degree, not only with respect to their temporal structure and right/left coordination, but also to changes in the song sequences according to the progress of courtship stridulation, even including accessory movements of other parts of the body. According to the complexity of their stridulatory behaviour ten gomphocerine species were chosen for this comparative study. The results indicate that the protocerebrum fulfils two important tasks in the control of stridulation: (1) it integrates sensory input relevant to stridulation that represents a certain behavioural situation and internal state of arousal, and (2) it selectively activates and deactivates the thoracic networks that generate the appropriate movement and sound patterns. With the knowledge of the natural behaviour and the accessibility to pharmacological and electrophysiological studies, the cephalic control system for stridulation in grasshoppers appears to be a suitable model for how the brain selects and controls appropriate behaviours for a given situation.