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Cicada Acoustic Communication. In: B. Hedwig (ed.), Insect Hearing and Acoustic Communication, Animal Signals and Communication 1, Springer-Verlag Berlin Heidelberg, pp.101-121.
Abstract
Cicadas are iconic insects that use conspicuously loud and often complexly structured stereotyped sound signals for mate attraction. Focusing on acoustic communication, we review the current data to address two major questions: How do males generate specific and intense acoustic signals and how is phonotactic orientation achieved? We first explain the structure of the sound producing apparatus, how the sound is produced and modulated and how the song pattern is generated. We then describe the organisation and the sensitivity of the auditory system. We will highlight the capabilities of the hearing system in frequency and time domains, and deal with the directionality of hearing, which provides the basis for phonotactic orientation. Finally, we focus on behavioural studies and what they have taught us about signal recognition.
... Lastly, while the AS (signals, auditory organs, and stridulatory devices) in other insect orders (e.g., Orthoptera, Hymenoptera, and Hemiptera) have been widely studied and associated with a wide range of biological behaviors and environmental factors, in bark beetles (Coleoptera: Curculionidae: Scolytinae), its integration with the chemical communication system, behavior, and reproductive ecology has received little attention [1,33,48,49]. In particular, it would be desirable for future studies focus on aspects related to acoustic signals, which, being apparently species-specific, could be involved in isolation and reproductive behavior, as well as in pheromone synthesis, especially in species that produce these compounds de novo. ...
Simple Summary
Simple Summary: Acoustic communication is present in different groups of insects and is used in different contexts during their life cycle. Bark beetles are a group of insects of ecological importance, because they can kill a large number of trees and affect forest succession These insects communicate using chemical signals for long distances, but while on or in the tree, they use acoustic communication to interact between individuals during the colonization of their host trees. A series of sounds have been described for bark beetles, which are produced by specialized anatomical structures under different conditions, such as stress, courtship, and territoriality. In this study, we worked with males of Dendroctonus adjunctus, and we described the stridulatory structures using optical and electron microscopy. In addition, we recorded and characterized the types of calls and their spectral and temporal characteristics under stress conditions, female–male, and male–male interactions. Results showed that the shape of the stridulatory apparatus is like males of other beetle species in the genus, and we identified single– and multi–noted calls with differences in temporal and spectral characteristics under three behavioral contexts. Finally, a new type of withdrawal call was identified in male–male interactions.
Abstract
The acoustic communication system (ACS) in bark beetles has been studied mainly in species of the genera Dendroctonus, Ips and Polygraphus. Specifically, ACS of the roundheaded pine beetle, Dendroctonus adjunctus, has been little studied. In this study, we described the stridulatory apparatus of this beetle using optical and scanning electron microscopy and recorded the call types produced by males in three behavioral contexts: stress, female–male–, and male–male interactions. From the spectrograms and waveforms, call types, as well as temporal (tooth strike, tooth strike rate, and intertooth strike interval) and spectral features (minimum, maximum and dominant frequency), were determined. Males have a functional elytro–tergal stridulatory apparatus—females do not—consisting of a file for the pars stridens and two lobes for the plectrum. Most of spectro–temporal features were statistically different between single– and multi–noted calls and across the three behavioral contexts. In the male–male interaction, a new type of call named “withdrawal” was produced by the male withdrawing or fleeing. Our results suggest that the spectro–temporal features of single– and multiple–noted calls in the three behavioral conditions are specific and different from each other. Yet, the combination of single and multiple calls determines an overall calling pattern characteristic of the tested behaviors and, therefore, is species–specific.
The presence of intra-specific acoustic communication in diurnal butterflies is not well established. Here, we examined the function of the tympanal ear (Vogel’s organ, VO) in the seasonally polyphenic butterfly Bicyclus anynana in the context of sexual signalling. We investigated how the VO and the flanking enlarged veins, which are suggested sound resonance chambers, scale with wing size across sexes and seasonal forms, and how disruptions to the VO alter courtship behaviour and mating outcomes. We found that males have VOs similar in size to females despite having smaller wings, and dry season (DS) male cubital and anal veins do not scale with the wing size. This suggests that the VO plays an important role in males and that cubital and anal veins in DS males may be tuned to amplify specific sound frequencies. Behavioural assays performed with deafened and hearing males of different seasonal forms, in pair and triad settings, showed that deafened DS males, but not wet season males, experienced lower mating success relative to their hearing counterparts. Our study documents a novel function for the wing tympanal membrane in mediating courtship and mating outcomes in diurnal butterflies.
Research in hearing sciences has provided extensive knowledge about how the human auditory system processes speech and assists communication. In contrast, little is known about how this system processes "natural soundscapes," that is the complex arrangements of biological and geophysical sounds shaped by sound propagation through non-anthropogenic habitats [Grinfeder et al. (2022). Frontiers in Ecology and Evolution. 10: 894232]. This is surprising given that, for many species, the capacity to process natural soundscapes determines survival and reproduction through the ability to represent and monitor the immediate environment. Here we propose a framework to encourage research programmes in the field of "human auditory ecology," focusing on the study of human auditory perception of ecological processes at work in natural habitats. Based on large acoustic databases with high ecological validity, these programmes should investigate the extent to which this presumably ancestral monitoring function of the human auditory system is adapted to specific information conveyed by natural soundscapes, whether it operate throughout the life span or whether it emerges through individual learning or cultural transmission. Beyond fundamental knowledge of human hearing, these programmes should yield a better understanding of how normal-hearing and hearing-impaired listeners monitor rural and city green and blue spaces and benefit from them, and whether rehabilitation devices (hearing aids and cochlear implants) restore natural soundscape perception and emotional responses back to normal. Importantly, they should also reveal whether and how humans hear the rapid changes in the environment brought about by human activity.
Meimuna opalifera males emit extremely complex calling songs, with the main section comprising two parts. To investigate whether these two parts of the calling song have different meanings for the receivers, we conducted playback experiments. We counted and compared the number of response calls when different types of sound stimuli were presented under laboratory conditions. Meimuna opalifera males emitted significantly greater response calls during the playback of stimuli containing the former part of the songs than those containing the latter part only. This suggests that M. opalifera males tend to respond by detecting characteristics in the former part of the songs. Because the peak frequencies were similar between the former and the latter parts, the temporal patterns of the songs might be important in short-range communication between males of M. opalifera.
Spatial capture–recapture (SCR) models are commonly used to estimate animal population density from detections and subsequent redetections of individuals across space. In particular, acoustic SCR models deal with detections of animal vocalisations across an array of acoustic detectors. Previously published acoustic SCR methods either estimate call density (calls per unit space per unit time) rather than animal density itself, require an independently estimated call rate to estimate animal density, or discard data from all but one detected call from each individual.
In this manuscript, we develop a new spatial capture–recapture model that estimates both call rate and animal density from the acoustic survey alone, without requiring an independently estimated call rate. Our approach therefore alleviates the need for the additional fieldwork of physically locating and monitoring individual animals. We illustrate our method and compare it to an existing approach using a simulation study and an application to data collected on an acoustic survey of the visually cryptic Cape peninsula moss frog Arthroleptella lightfooti .
In the context of our acoustic survey, our calling animal density estimator has low bias, good precision and confidence intervals with appropriate coverage, yielding results that are consistent with previous studies of the same species.
Our method can obtain accurate and precise estimates of animal density while eliminating the fieldwork burden associated with separately estimating call rate. We discuss how the development of our model's likelihood reveals a clear path to further extensions, which may incorporate features such as animal movement processes and uncertain individual identification.
This work introduces a new approach for automatic identification of crickets, katydids and cicadas analyzing their acoustic signals. We propose the building of a tool to identify this biodiversity. The study proposes a sound parameterization technique designed specifically for identification and classification of acoustic signals of insects using Mel Frequency Cepstral Coefficients (MFCC) and Linear Frequency Cepstral Coefficients (LFCC). These two sets of coefficients are evaluated individually as has been done in previous studies and have been compared with the fusion proposed in this work, showing an outstanding increase in identification and classification at species level reaching a success rate of 98.07% on 343 insect species.
Context
While remote sensing imagery is effective for quantifying land cover changes across large areas, its utility for directly assessing the response of animals to disturbance is limited. Soundscapes approaches—the recording and analysis of sounds in a landscape—could address this shortcoming.
Objectives
In 2011, a massive wildfire named “the Horseshoe 2 Burn” occurred in the Chiricahua National Monument, Arizona, USA. We evaluated the impact of this wildfire on acoustic activity of animal communities.
Methods
In 2013, soundscape recordings were collected over 9 months in 12 burned and 12 non-burned sites in four ecological systems. The seasonal and diel biological acoustic activity were described using the “Bioacoustic Index”, a detailed aural analysis of sound sources, and a new tool called “Sonic Timelapse Builder” (STLB).
Results
Seasonal biophony phenology showed a diurnal peak in June and a nocturnal peak in October in all ecological systems. On June mornings, acoustic activity was lower at burned than at non-burned sites in three of four ecological systems, due to a decreased abundance of cicadas directly impacted by the death of trees. Aural analyses revealed that 55% of recordings from non-burned sites contained insect sounds compared to 18% from burned sites. On October nights, orthopteran activity was more prevalent at some burned sites, possibly due to post-fire emergence of herbaceous.
Conclusions
Soundscape approaches can help address long-term conservation issues involving the responses of animal communities to wildfire. Acoustic methods can serve as a valuable complement to remote sensing for disturbance-based landscape management.
Detection of substrate vibrations is an evolutionarily old sensory modality and is important for predator detection as well as for intraspecific communication. In insects, substrate vibrations are detected mainly by scolopidial (chordotonal) sense organs found at different sites in the legs. Among these sense organs, the tibial subgenual organ (SGO) is one of the most sensitive sensors. The neuroanatomy and physiology of vibratory sense organs of cicadas is not well known. Here, we investigated the leg nerve by neuronal tracing and summed nerve recordings. Tracing with Neurobiotin revealed that the cicada Okanagana rimosa (Say) (Hemiptera: Cicadidae) has a femoral chordotonal organ with about 20 sensory cells and a tibial SGO with two sensory cells. Recordings from the leg nerve show that the vibrational response is broadly tuned with a threshold of about 1 m/s2 and a minimum latency of about 6 ms. The vibratory sense of cicadas might be used in predator avoidance and intraspecific communication, although no tuning to the peak frequency of the calling song (9 kHz) could be found.
The functions of female song found in a few cicadas have rarely been studied. In the cicada Subpsaltria yangi we investigated the acoustic behaviour and signal structure of songs produced by females, the phonotaxis of males, and mate choice, as well as the selective pressure imposed on this species by predators. Pair-formation in S. yangi occurs when males signal, females respond, then males move to signaling females, which is opposite to that in most other cicadas where females move to calling males. Females only mate once and are sexually unreceptive after copulation. Most males mate once, but ~25% mate multiply. Females display little direct evidence of mate preference or choice of males, and all mate encounters led to a successful mating. Only males are attacked by a robber fly, Philonicus albiceps, while flying to females. This imposes strong selection on males – only males who can evade predators mate. Males are also attracted to human simulations of female calls. This behaviour exposes the mating system to impacts from anthropogenic noise systems which could disrupt mating activity of this species. Our results improve the understanding of mate choice/competition in cicadas, and are valuable for future studies of the evolution of sound communication in the Cicadoidea.
The acoustic communication of grasshoppers, crickets, and katydids provides prime examples of general principles of how nervous systems represent sensory information. The processing of auditory signals in insects is innate; thus the involved neuronal modules are “hardwired.” In addition, the relevant stimulus space is restricted, facilitating the investigation. A major problem of sensory processing is the trial-to-trial variability of spike trains caused by the stochastic opening and closing of ion channels. In animals that can spend only a few neurons for a given task, this unreliability of spike trains is a relevant constraint for neuronal encoding.
Signal recognition in insects depends primarily on features of the sound envelope, the pattern of amplitude modulations. The receptor neurons respond with high temporal precision and reflect the stimulus’s envelope in their spike patterns. This kind of “temporal code” is later transformed to a “labeled line code” representation in which single neurons encode specific sound features. Similarly to the larger nervous systems of vertebrates, at this stage, spike rates are reduced and the presence of particular sound features can be read out from a population code. Remarkably, in insects, the sparsening and change of coding schemes occur already within a few synapses after the receptors.
Modeling studies suggest how feature detectors equipped with linear filters may explain behavioral scores found with specific stimulus variations. Remarkably, in grasshoppers and crickets, the filters found by this approach resembled Gabor filters, which allow an easy transition between behavioral preference functions found in different species.
The sense of hearing contributes importantly to an animal’s fitness. It allows detection of predators and prey and communication with conspecifics even in the dark and over large distances. Hearing organs evolved in about 20 groups of insects. Hearing is used by moths and other insects for avoiding predatory bats; by cicada, crickets/bushcrickets, moths, and grasshoppers for intraspecific communication; and by parasitic flies to locate singing hosts. Despite the variety of these insect groups, the neural processing of sound signals faces very similar fundamental challenges related to signal detection, directional processing, frequency discrimination, pattern recognition, and coping with self-generated noise. Solutions to these problems are implemented by specific network, cellular, and synaptic properties of neural circuits. Owing to their rather simple organization, insect auditory pathways can be explored and analyzed at the level of identified neurons to reveal fundamental mechanisms of auditory processing.
Compared to all other hearing animals, insects are the smallest ones, both in absolute terms and in relation to the wavelength of most biologically relevant sounds. The ears of insects can be located at almost any possible body part, such as wings, legs, mouthparts, thorax or abdomen. The interaural distances are generally so small that cues for directional hearing such as interaural time and intensity differences (IITs and IIDs) are also incredibly small, so that the small body size should be a strong constraint for directional hearing. Yet, when tested in behavioral essays for the precision of sound source localization, some species demonstrate hyperacuity in directional hearing and can track a sound source deviating from the midline by only [Formula: see text]-[Formula: see text]. They can do so by using internally coupled ears, where sound pressure can act on both sides of a tympanic membrane. Here we describe their varying anatomy and mode of operation for some insect groups, with a special focus on crickets, exhibiting probably one of the most sophisticated of all internally coupled ears in the animal kingdom.
Insect ears evolved many times independently. As a consequence, a striking diversity exists in the location, construction and behavioural implementation of ears. In this review, we first summarise what is known about the evolutionary origin of ears and the presumed precursor organs in the various insect groups. Thereafter, we focus on selective forces for making and keeping an ear: we discuss detecting and localising predators and conspecifics, including establishing new "private" channels for intraspecific communication. More advanced aspects involve judging the distance of conspecifics, or assessing individual quality from songs which makes auditory processing a means for exerting sexual selection on mating partners. We try to identify negative selective forces, mainly in the context of energy expenditure for developing and keeping an ear, but also in conjunction with acoustic communication, which incorporates risks like eavesdropping by predators and parasitoids. We then discuss balancing pressures, which might oppose optimising an ear for a specific task (when it serves different functions, for example). Subsequently, we describe various scenarios that might have led to a reduction or complete loss of ears in evolution. Finally, we describe cases of sex differences in ears and potential reasons for their appearance.
The efficiency of long-distance acoustic signalling of insects in their natural habitat is constrained in several ways. Acoustic signals are not only subjected to changes imposed by the physical structure of the habitat such as attenuation and degradation but also to masking interference from co-occurring signals of other acoustically communicating species. Masking interference is likely to be a ubiquitous problem in multi-species assemblages, but successful communication in natural environments under noisy conditions suggests powerful strategies to deal with the detection and recognition of relevant signals. In this review we present recent work on the role of the habitat as a driving force in shaping insect signal structures. In the context of acoustic masking interference, we discuss the ecological niche concept and examine the role of acoustic resource partitioning in the temporal, spatial and spectral domains as sender strategies to counter masking. We then examine the efficacy of different receiver strategies: physiological mechanisms such as frequency tuning, spatial release from masking and gain control as useful strategies to counteract acoustic masking. We also review recent work on the effects of anthropogenic noise on insect acoustic communication and the importance of insect sounds as indicators of biodiversity and ecosystem health.
Males of the North American cicada Okanagana rimosa (Homoptera: Cicadidae, Tibicininae) emit loud airborne acoustic signals for intraspecific communication. Specialised vibratory signals could not be detected; however, the airborne signal induced substrate vibrations. Both auditory and vibratory spectra peak in the range from 7-10 kHz. Thus, the vibrations show similar frequency components to the sound spectrum within biologically relevant distances. These vibratory signals could be important as signals involved in mate localization and perhaps even as the context for the evolution of the ear in a group of parasitoid flies.
SYNOPSIS. Vibration through the substrate has likely been important to animals as a channel of communication for millions of years, but our awareness of vibration as biologically relevant information has a history of only the last 30 yr. Morphologists know that the jaw mechanism of early amphibians allowed them to perceive vibration through the substrate as their large heads lay on the ground. Although the exact mechanism of vibration production and the precise nature of the wave produced are not always understood, recent technical advances have given answers to increasingly sophisticated questions about how animals send and receive signals through the substrate. Some of us have been forced to explore the use of vibration when all other attempts to manipulate animals in the field have failed, while others began to think about vibration to explain some of the puzzling behaviors of species they were studying in other contexts. It has thus become clear that the use of vibration in animal communication is much more widespread than previously thought. We now know that vibration provides information used in predator-prey interactions, recruitment to food, mate choice, intrasexual competition and maternal/brood social interactions in a range of animals from insects to elephants.
The songs of Aleeta curvicosta, Tryella castanea, T. crassa, T. kauma and T. rubra are analysed. Differences between the songs of the five species are discussed in addition to differences across the distribution of species and within populations. Timbal action of all four Tryella species was found to be similar to that of Aleeta curvicosta, that is a single muscle contraction produces multiple sound pulses as each rib of the timbal buckles. A corrigenda to a recent review of the systematics of these genera (Moulds 2003) is provided.
The vertebrate ear can analyse the frequency components of sound with high
resolution, recognizing complex acoustic signals even against a noisy background
Parameters of the calling song that were necessary to evoke phonotaxis in female bladder cicadas (Cystosoma saundersii) were determined for both long-range and short-range communication between the sexes.
Females flew to loudspeakers that were broadcasting model calling songs that resembled the natural calling song of the males. They also initiated courtship in response to the model calling songs. When flying females were offered a choice between a model resembling the natural song in all parameters (the control model) and a model in which one of the temporal parameters had been changed (the experimental model), they were attracted equally to the control and experimental models. When the carrier frequency of the experimental model was changed, the females were attracted exclusively to the control model. When the same model calling songs were presented to tethered, flying females in the laboratory, they turned only towards models with a carrier frequency close to that found in the natural song. Changing the temporal parameters of the model did not affect either the turning preferences of the females or their reaction times. When the same series of control and experimental models were played, one at a time, to caged females in the laboratory, courtship responses were elicited only by models with temporal parameters similar to those of the natural song. In contrast, a wide range of carrier frequencies was found to elicit courtship, provided that the temporal parameters were similar to those of the control. It is concluded that, in C. saundersii, identification of conspecific males by females is a two-stage process, with the carrier frequency of the male calling song being more important in long-range communication (flight) and the temporal parameters of the calling song being more important in short-range communication (courtship).
The fauna of singing cicadas (Cicadoidea) of Romania has been investigated on a single field excursion in 2004 with classic and bioacoustic methods, using recording equipment for sonic range and ultrasonic detectors. Nine species were recorded for Romania in the past: Lyristes plebejus (Scopoli 1763), Cicada orni Linnaeus 1758, Cicadatra atra (Olivier 1790), Cicadetta tibialis (Panzer 1798), Cicadetta montana s. lat. (Scopoli 1772), Cicadetta podolica (Eichwald 1830), Pagiphora annulata (Brulle 1832), Tettigetta brullei (Fieber
1876), and Tibicina haematodes (Scopoli 1763). We discovered 3 additional species: Cicadatra hyalina (Fabricius 1798), Cicadetta brevipennis Fieber 1876, and Cicadetta iphigenia Emeljanov 1996. These are the first records for Romania, for Cicadetta iphigenia this is also the first record outside the Krimean Peninsula.
The fauna of singing cicadas (Cicadoidea) of Macedonia has been investigated with classic and bioacoustic methods, using recording equipment for sonic range and ultrasonic detectors. In the literature we found data for 6 species, but the reported locality of Tibicina steveni (Krynicki, 1837) is in Bulgaria. In addition to the remaining 5 species: Lyristes plebejus (Scopoli, 1763), Cicada orni Linné, 1758, Tibicina haematodes (Scopoli, 1763), Cicadatra atra (Olivier, 1790) and C. hyalina (Fabricius, 1798), we discovered in Macedonia 10 more species: Cicadatra platyptera Fieber, 1876, C. persica Kirkaldy, 1909, Tettigetta brullei (Fieber, 1876),
T. dimissa (Hagen, 1856), Cicadetta montana (Scopoli, 1772), C. cerdaniensis Puissant & Boulard, 2000, C. macedonica Schedl, 1999, C. cf. podolica (Eichwald, 1830), C. tibialis (Panzer, 1798) and Pagiphora annulata (Brullé, 1832). The distribution of species is shown in maps with UTM grid. Additional new bioacoustic
data for Cicadatra platyptera and P. annulata are included.
Playback experiments with natural and modified signals broadcast to specimens of Cicada orni Linnaeus 1758 were performed in order to understand selective singing responsiveness by males during acoustic chorus activity. Males showed different patterns of response to different kinds of signals. Frequently heterospecific calling signals did not elicit effective response but in several instances they were perceived as appropriate, and males replied to them. This was the case of calling song of Cicada mordoganensis Boulard 1979 which proved to be as effective as the proper song of C orni Modification in the time domain showed that males basically need to hear a minimum signal duration (echeme and interval duration) corresponding to the lowest limit of natural variation in the species. Results supported the idea that males seem to perceive variation in signals in a discontinuous manner and are unable to show selective responsiveness to small differences. Such apparent tolerance and permissiveness in male singing response to heterospecific calling songs may result from lack of selection on the response to allopatric-heterospecific signals.
Acoustic methods have been used to investigate the biodiversity of cicadas in Peninsular Malaysia. Various approaches and methods are described how to match the species with the recorded songs in nature. As a result the song pattern and characteristics of seven cicada species are presented. Songs of 4 species are described for the first time (Dundubia euterpe, Chremistica guamusangensis, Chremistica pontianaka and Huechys sanguinea) and songs of 3 species were almost simultaneously published by M. Boulard from localities in Thailand (Dundubia oopaga, Pomponia pendleburyi, Cryptotympana aquila). Our data from Malaysia are in agreement with his description.
The cicada fauna from Portugal is reviewed, as a result of a joint Portuguese-French project. Thirteen species are reported (Lyristes plebejus, Cicada orni, Cicada barbara lusitanica, Tibicina tomentosa, Tibicina quadrisignata, Tibicina garricola, Melampsalta varipes, Tympanistalna gastrica, Euryphara contentei, Tettigetta argentata, Tettigetta estrellae, Tettigetta josei, Tettigetta mariae), while five taxa which were previously referred to in the literature, have not been found (Tibicina corsica fairmairei, Tibicina haematodes, Tibicina nigronervosa, Cicadetta flaveola, Cicadivetta tibialis). Based on morphological and acoustic features, the following synonymies are established: Tettigetta argentata (Olivier, 1790) = Tettigetta atra (Gomez-Menor, 1957) n. syn. and Tettigetta estrellae Boulard, 1982 = Tettigetta septempulsata Boulard & Quartau, 1991 n. syn. Data on time of emergence, geographical distribution, habitat occupation and acoustic calling behaviour are given for each species.
Electromyograms (EMGs) of the timbal muscles were recorded during the calling songs and ‘protest songs’ (also referred to as alarm signals) in five species of cicadas: Cicada barbara lusitanica, Tettigetta josei, Tettigetta argentata, Tibicina quadrisignata and Tympanistalna gastrica.The timbal muscle contraction rates of all species ranged from 50 to 250 Hz. The basic timbal cycle generating sound during the inward and outward buckling of the timbal was maintained in calling song and protest song for all five species. Comparison of the temporal parameters and the corresponding timbal muscle activity in both sound signals revealed that the timbal muscle period as well as the intertimbal delay showed the same mean values. Major differences between calling song and protest song are apparent in the pattern determining echemes and phrases as well as in the sound amplitude modulation.The amplitude of the sound pulse during the inward movement of the timbal was positively correlated with the time lag from the timbal muscle activity to the IN sound pulse in the calling songs of Tettigetta josei, Tettigetta argentata and Tympanistalna gastrica, species with a one-to-one correspondence between a single contraction of the timbal muscle and the production of a sound pulse as the timbal buckles inwards. These relationships did not hold for the other two species, where a single contraction of the timbal muscle causes the timbal to buckle inwards in steps to produce a train of sound pulses. This indicates the presence of different mechanisms responsible for sound amplitude modulation. There was no evidence that the period of the timbal muscle contractions correlated with changes in sound pulse amplitude during singing.
The sexual behaviors of Okanagana canadensis (Provancher) and O. rimosa (Say) are described. In northern Michigan, O. canadensis is typically found in coniferous vegetation, such as cedars; whereas O. rimosa frequent deciduous vegetation. In both species, males call from stationary perches, and females approach them. Females have no specialized receptivity signals, but both males and females engage in bouts of wing flicking that may be alternative, low-risk signaling. Mating is brief and involves no elaborate courtship. The Okanagana mating system, characterized by male advertisement and female searching, is contrasted with that of Magicicada spp., the periodical cicadas of North America, and discussed in the context of relative risks of signaling and searching behaviors.
Detailed descriptions of the acoustic signals of European cicadas are available only for a few species. In this paper the acoustic signals and biomechanics of the timbals in nine species of cicadas from Portugal have been examined. Those species are Cicada barbara lusitanica (Boulard, 1982), C. orni (Linnaeus, 1758), Tettigetta argentata (Olivier, 1790), T. atra (Gomez-Menor, 1957), T. estrellae (Boulard, 1982), T. josei (Boulard, 1982), Tibicina quadrisignata (Hagen, 1855), Tympanistalna gastrica (Stal, 1854), and one unidentified species of Tettigetta. A qualitative and quantitative description of the sound is given in the time domain and the frequency domain. An acoustic male-to-male interaction signal that ceases the courtship was identified in C. barbara lusitanica. Some evolutionary aspects related to the biomechanics of the timbals and to the sounds produced are discussed.
Periodical cicada (Magicicada spp.) sexual pair formation takes place in dense aggregations and involves intense male-male competition for limited mating opportunities. Pair-forming behavior in these species has been poorly understood because of limited knowledge of sexual communication. We have found that sexually receptive female Magicicada ick their wings in timed response to an individual chorusing male; this previously unrecognized female response is hereafter referred to as a 'wing-ick' signal. We document the nature, timing, and species-speci city of this signal as well as its absence in both immature and mated females. We also document changes in male chorusing and searching behavior in response to wing-ick signals and male responses to the signals' visual and acoustical components. We test the hypothesis that female sensory psychology has shaped the evolution of -decim calls by 1) Chris Simon. This work represents parts of doctoral theses submitted by both authors in partial ful llment for doctoral degrees from the Horace Rackham School of Graduate Studies, The University of Michigan. c ° Koninklijke Brill NV, Leiden, 2001 Behaviour 138, 827-855 828 COOLEY & MARSHALL favoring frequency-modulated male calls that are more readily distinguishable in an intense background chorus. Within mating aggregations, male Magicicada attempt to usurp ongoing courtships and also engage in interference competition by acoustically obscuring the calls of potential interlopers, reducing the likelihood of a female response.
Acoustic mate-attracting signals of related sympatric, synchronic species are always distinguishable, but those of related allopatric species sometimes are not, thus suggesting that such signals may evolve to “reinforce” premating species isolation when similar species become sympatric. This hypothesis predicts divergences restricted to regions of sympatry in partially overlapping species, but such “reproductive character displacement” has rarely been confirmed. We report such a case in the acoustic signals of a previously unrecognized 13-year periodical cicada species, Magicicada neotredecim, described here as a new species (see Appendix). Where M. neotredecim overlaps M. tredecim in the central United States, the dominant male call pitch (frequency) of M. neotredecim increases from approximately 1.4 kHz to 1.7 kHz, whereas that of M. tredecim remains comparatively stable. The average preferences of female M. neotredecim for call pitch show a similar geographic pattern, changing with the call pitch of conspecific males. Magicicada neotredecim differs from 13-year M. tredecim in abdomen coloration, mitochondrial DNA, and call pitch, but is not consistently distinguishable from 17-year M. septendecim; thus, like other Magicicada species, M. neotredecim appears most closely related to a geographically adjacent counterpart with the alternative life cycle. Speciation in Magicicada may be facilitated by life-cycle changes that create temporal isolation, and reinforcement could play a role by fostering divergence in premating signals prior to speciation. We present two theories of Magicicada speciation by life-cycle evolution: “nurse-brood facilitation” and “life-cycle canalization.”
1. In Cystosoma saundersii sound is generated by collapse of a pair of tymbals and radiated by a large, resonant, air-filled abdomen. Each tymbal comprises a flexible, biconvex membrane bearing seven long ribs. Tymbal collapse is caused by contraction of a large tymbal muscle, which acts on the tymbal plate. Each tymbal muscle is innervated by one motor neurone.
2. A single collapse of a tymbal produces two distinct pulses of sound, one when rib 1 buckles and one when ribs 2-4 buckle. A quieter sound is produced when the ribs click outwards.
3. A slowly contracting tensor muscle increases the convexity and stiffness of the tymbal, resulting in a reduction in the delay between the first and second sound pulse and in louder pulses.
4. Protest songs contain features of other songs. There is a delay between the spike in one tymbal motor neurone and its partner, and hence between sound produced by one tymbal and the other, of one-quarter of the interval between spikes in one motor neurone alone.
5. Calling songs are produced by males at dusk. Sound pulses have a smooth envelope and are very loud as a result of contraction of the tensor muscles and extension of the abdomen.
6. Courtship songs are triggered in a calling male by the presence of a female. Song is quite quiet, and broken into short chirps.
SUMMARY 1. The male cicada, Okanagana vanduzeei, produces a calling song with a pulse repetition frequency of 550 Hz. This sound is produced by a pair of tymbals, each of which is buckled by a large tymbal muscle. Males sing in full sun and the operating temperature of the tymbal muscles is 40-45 °C. 2. Analysis of the songs of animals with the tymbal mechanism destroyed on one side, and of the sounds produced by directly manipula- ting a tymbal, indicates that the two tymbals normally buckle synchro- nously and that only one sound pulse is produced per tymbal muscle contraction. This implies that the contraction frequency of each tymbal muscle is 550 Hz. 3. Recordings of calling songs from animals with implanted electrodes show that there is usually synchrony between left and right tymbal muscle contractions and that each tymbal muscle can operate at a frequency of about 550 Hz. The recordings also show that there is a 1:1 correlation between muscle electrical and mechanical activity, i.e. these muscles are synchronous and not asynchronous muscles. 4. The ultrastructure of the tymbal muscle is clearly that of a very fast, synchronous muscle: the myofibrils are small, the sarcoplasmic reticulum is extraordinarily well developed, and the T-tubules lie at the 1/4 and 3/4 positions along the sarcomere. 5. When set up for isometric recording, with their nerve supply severed, the tymbal muscles often show spontaneous electrical and mechanical oscillations. The frequency of these oscillations is strongly temperature dependent, and at higher temperatures approaches the normal operating frequency of the muscle. The tendency to oscillate is so *This paper is dedicated to the late Professor J. W. S. Pringle who was a pioneer in studies of cicada muscles and a major contributor to our understanding of insect muscle in general. We think he would have enjoyed the new perspective given by the tymbal muscles of Okanagana vanduzeei.
Many books from symposia describe the current status in well established fields of research, where much is known and where the loose ends are only details in the picture. The topic dealt with here does not fall into this pattern. The study of time as a parameter in its own right is difficult, and the loose ends tend to do minate the present picture. Although the book does provide the reader with an overview of the field, its main value is probably to act as a source of "food for thought" for those interested in the function of sense organs and nervous systems as substrates for behaviour. The Introduction is intended to provide the readers of the book with a short guide to the topiCS discussed in the different chapters. The rather detailed Index may help those looking for information on specific topiCS. The Index also explains most of the abbreviations used in the book. The basic idea of the Danavox symposia is to invite a small group of experts to discuss a rather narrow theme in sound communication. The small number of active par tiCipants has the advantage of encouraging intense dis cussions and of avoiding overloading the program. On the other hand, selecting the partiCipants is difficult.
Periodical cicadas, Magicicada septendecim and M. cassini, occupy the same habitat and the males’ singing overlaps, often forming a chorus, which in M. cassini is synchronized. The calling songs of the males differ in their sound frequency spectra and in the temporal pattern. Playback of conspecific calling songs in the field initiated singing in both species. In M. cassini the initial tick part of the song stimulated males to synchronize their songs with the chorus; the final buzz part attracted preferably females by flight phonotaxis.
For efficient acoustic communication precise concordance between the properties of sound signals of emitters and those of the auditory system of receivers is necessary. An extremely important parameter, the communication range, directly depends on it. So, for any species this concordance is highly “desirable”. Sound-producing and sound-receiving systems have different morphological substrate, are controlled by different genes and matching between them is established by natural selection as the result of a complicated game of different selection forces fitting the animal as a whole to definite environment. The degree of concordance between hearing and sound production vary greatly in different animals and is dependent on the presence or absence of forces working against it.
The auditory threshold of Cyclochila australasiae, recorded in the whole auditory nerve, is lowest at 3.5 kHz. The roll-off between 4 and 8 kHz is very steep, with thresholds above 96 dB at 8 kHz and higher. The auditory curve is more sharply tuned in males than in females. Experimental manipulations designed to alter the mechanical properties of the accessory structures of the auditory system, and also the auditory organ, suggest that the observed tuned auditory response is not due to resonance of the abdominal air sac, the tympana, the tympanal apodeme, or the auditory organ. The tensor nerve of Cyclochila australasiae responds to acoustic stimuli with a summed response similar to that seen in the auditory nerve. This response probably originates at the tymbal and tensor chordotonal organs, and is independent of the auditory nerve response. The threshold of the tensor nerve response is 15 to 20 dB less sensitive than that of the auditory nerve, but is similarly tuned to 3.5 kHz. The tuning of the auditory threshold of Cyclochila australasiae appears to be due to intrinsic properties common to the scolopidia of the auditory organ and those of the tymbal and tensor chordotonal organs.
The neuromuscular mechanism of sound-production in cicadas has been elucidated by a detailed anatomical and physiological study of Platypleura capitata (Oliv.) and by the analysis of magnetic tape recordings of the song of eight other species in Ceylon. In all cases the song consists of a succession of pulses, the repetition frequency being between 120 and 600/sec. Each pulse is composed of a damped train of sound waves whose frequency is determined by the natural period of vibration of the tymbals. A pulse of sound is emitted when the tymbal suddenly buckles or is restored to its resting position by its natural elasticity; in the song of some species both movements are effective. The tymbal muscles, which are responsible for the buckling, have a myogenic rhythm of activity, initiated, but only slightly controlled in frequency, by impulses in the single nerve fibre supplying each muscle. The two tymbals normally act together. The curvature of the tymbals can be increased by the contraction of accessory muscles, the chief of which are the tensor muscles. This increases the volume of sound emitted at each click and lowers the pulse repetition frequency; the abdomen is raised from the opercula by contraction of the tensor muscles. The tracheal air sacs form a cavity which is approximately resonant to the frequency of tymbal vibration and can be varied in size by expansion of the abdomen. Cicada songs, to the human ear, appear to be of great variety. The differences arise largely from the properties of the mammalian cochlea as a frequency analyser; the degree of coherence of phase between pulses, which is probably without significance to the insect, is of great importance in determining the quality of the sound to a human observer. The songs of three species which resemble respectively a bell, a musical phrase and a strident chatter are analysed from high-speed oscillograms, and the difference in quality of sound is explained by reference to the wave-forms. Some species emit a regular succession of pulses. Others have a slow pattern to their song, produced by the co-ordinated nervous excitation of three functional groups of muscles: (a) wthe tymbal muscles, producing the sound; (b) the tensor muscles, controlling the amplitude and pulse repetition frequency; (c) the muscles controlling the resonance of the air sacs. Of the nine species recorded in Ceylon, those belonging to the genus Platypleura produce their pattern by using (b) and (c), the tymbal muscle being in continuous rhythmic activity; those of the genus Terpnosia use mainly (a) to interrupt the continuity of emission of sound pulses, with some accompanying change in amplitude and pulse frequency. The remaining species use all three muscle groups, but different patterns of co-ordination produce great differences in song. In one species (Platypleura octoguttata) a distinct courtship song was recorded from a male in close proximity to a female; this ends with attempted copulation. Preliminary electrophysiological experiments show that the chordotonal sensilla associated with the tympana are extremely sensitive to high-pitched sounds. When the song of another cicada is played back through a loudspeaker the impulse pattern in the auditory nerve corresponds to the pulse modulation envelope, with some after-discharge, as in other insect ‘ears’ (Pumphrey, 1940). The function of the song is to assemble the local population of a cicada species (males and females) into a small group. It remains to be determined whether it is the main intersexual stimulus in mating behaviour.
Acoustic communication as evolved in insects, amphibians, birds and mammals mainly serves to bring the sexes together for successful reproduction. Sound signals, most commonly emitted by one sex, play a major role in this communication process. But one should not neglect vibrational, visual and chemical signals associated with communicative behavior in the natural environment. Diurnally active cicadas — for example, the periodical cicadas (Magicicadidae) — are guided in their daily flights by visually recognized landmarks (bushes, trees), and they choose those landing sites at which conspecific males are singing (Alexander and Moore 1962, Huber 1983a). In the Australian bladder cicada, Cystosoma saundersii (Westwood) which is active at dusk, flight phonotaxis in the female is mainly guided by acoustical cues (Doolan 1982). Visual and acoustical signals emitted by the sexual partner establish pair formation in many acridid grasshoppers (Jacobs 1953, Riede et al. 1979, Riede 1982).
1. In Cystosoma saundersii sound is generated by collapse of a pair of tymbals and radiated by a large, resonant, air-filled abdomen. Each tymbal comprises a flexible, biconvex membrane bearing seven long ribs. Tymbal collapse is caused by contraction of a large tymbal muscle, which acts on the tymbal plate. Each tymbal muscle is innervated by one motor neurone. 2. A single collapse of a tymbal produces two distinct pulses of sound, one when rib 1 buckles and one when ribs 2-4 buckle. A quieter sound is produced when the ribs click outwards. 3. A slowly contracting tensor muscle increases the convexity and stiffness of the tymbal, resulting in a reduction in the delay between the first and second sound pulse and in louder pulses. 4. Protest songs contain features of other songs. There is a delay between the spike in one tymbal motor neurone and its partner, and hence between sound produced by one tymbal and the other, of one-quarter of the interval between spikes in one motor neurone alone. ^r-Galting songs are produced by males at dusk. Sound pulses have a smooth envelope and are very loud as a result of contraction of the tensor muscles and extension of the abdomen. 6. Courtship songs are triggered in a calling male by the presence of a female. Song is quite quiet, and broken into short chirps.
Effective communication requires that the receiver not only detect the presence of a signal but also discriminate significant variations in signals. Consequently, both attenuation and degradation of the structure of acoustic signals during transmission will limit the range of communication. In this study we document two primary sources of degradation of acoustic signals during propagation through natural environments, irregular amplitude fluctuations and reverberations. Amplitude fluctuations arise especially from atmospheric turbulence, while reverberations also result from scattering surfaces, such as vegetation. Both primarily mask information coded in amplitude modulation of the signal and repetitive frequency modulation, like the trills in the songs of many passerine birds. Irregular amplitude fluctuations primarily mask low frequencies of amplitude modulation in signals. Atmospheric turbulence from wind is the primary determinant of the intensity of irregular amplitude fluctuations, although amplitu...
The tympanic organ of the Cicadidae is situated on the abdominal ventral side stretching inside a cuticular capsule, which is formed as an irregular cone-shaped protuberance on both sides of the second abdominal segment. Near the hearing capsule lies the drum in a cavity spanned perpendicularly with regard to the longitudinal axis of the animal. The drum forms a narrow and flat process reaching in the hearing capsule. The tympanic organ is attached to this cuticular body. On the other side the organ is fixed at the integument of the distal part of the hearing capsule. There are two protuberances, to which the scolopidia are fastened.
The tympanic organ consists of about 1300 scolopidia each composed of the following distinct cells: the sense cell, which distally bears the cilium, the proximal attachment cell, the scolopale cell, the cap cell, and a distal attachment cell. Proximal and distal attachment cells mediate the attachment of the organ at the epidermal cells of the cuticle. Numerous folds and much desmosomes associated with microtubules fasten the cells at each other so that the organ is spanned very tightly between the two cuticular bodies.
The auditory organ of Cystosoma saundersii consists of 2000-2200 scolopidia arranged in two groups, a dorsal and a ventral group. The dorsal group contains scolopidia orientated along the longitudinal axis of the organ while the ventral group contains scolopidia aligned at right angles to these. On the basis of current theories of sensory transduction, it is possible that these groups may have different intensity characteristics. The cellular composition of an individual scolopidium was described at the electron microscope level and was found to be similar to that occurring in most other chordotonal organs. Slight differences in fine structure were observed in the structure of the scolopale, the mass and position of the ciliary dilatation and the ciliary root. Differences in these parameters may influence the adequate stimulus needed for a chordotonal organ. The fine structure of proximal and distal attachments of the scolopidia to the cuticle is similar to that of muscle attachments observed in insects, crustaceans and arachnids. The central projections of the auditory nerve within the thoracic ganglia are similar to those described for the periodical cicadas.
The cochlea analyses the spectral content of complex sounds so that the amplitude of each frequency component is encoded in a separate set of sensory neurones. The frequency analysis is accomplished in different vertebrates both by the graded mechanical characteristics of the cochlear partition and by the intrinsic properties of the sensory receptors, the hair cells. In one mechanism found in lower vertebrates, the hair cell membrane is tuned by an electrical resonance which arises from an interaction of a voltage-dependent Ca2+ conductance and a Ca2+-activated K+ conductance. This review examines the evidence for such a mechanism and discusses how the attributes of the membrane conductances are varied to produce a distribution of resonant frequencies covering the auditory range.
of single descending axons [4]. In these experiments constant stimulus trains were sufficient to elicit singing. This is evidence for specific descending brain neurons in crickets, which might function as tonically active command neurons [5] for the control of singing behaviour. Corresponding neurons have recently been identified for the control of stridulation in acridid grasshoppers [6]. In summary, the experiments performed so far on cricket stridulation have left unresolved whether the chirp rhythm is determined by patterned activity from the brain or is controlled by descending tonic discharge. Also, the relevant neurons remain unknown. To answer these questions I sought to identify interneurons in the brain of the cricket Gryllus bimaculatus which evoke stridulation when stimulated. Intracellular recordings were obtained in the medial protocerebrum, a region in which electrical stimulation of the neuropil is known to elicit singing behaviour. Experiments were performed with tethered crickets, which were free to move their wings. Wing movements were measured with an optoelectronic system [7]. The movement also reflected the sound pattern during singing (Fig. 1B, inset). Hundreds of intracellularly impaled neurons in the protocerebrum of G. bimaculatus were depolarized during the course of the recordings, and the effect of the increased discharge rate on the behaviour was observed. An interneuron was encountered eight times which evoked stridulation of calling song when depolarized. Its arborization pattern in the brain was stained in three experiments. The interneuron (Fig. 1A) has a soma position close to the midline at the dorsal surface of the protocerebrum. The primary neurite projects ventrally and then turns posteriorly. At this point it sends off lateral arborizations. Other branches run almost parallel to the
1.The calling song ofMagicicada cassini consists of complex pulses of sound, each pulse being subdivided into about 9 sub-pulses, and is broadly tuned (Q3 dB = 5) around a peak frequency near 6 kHz. The calling song ofM. septendecim consists of a modulated pure tone, not divided into pulses or sub-pulses, and is sharply tuned (Q3 dB = 25) at a peak frequency of 1.3 kHz (Figs. 2, 3).2.In bothM. cassini andM. septendecim the sound-producing tymbal consists of a membrane bearing 12 stiffening ribs anteriorly and an irregularly shaped tymbal plate posteriorly. The tymbal ofM. cassini has a much higher resting stiffness than that ofM. septendecim.3.The tymbal muscles of both species produce single twitches in response to electrical stimulation and contract more rapidly as muscle temperature increases (Fig. 6). The tymbal muscle ofM. cassini is relatively more powerful than that ofM. septendecim.4.InM. cassini, each cycle of tymbal movement produces one complex pulse, the succession of 9 sub-pulses being correlated with the successive buckling of 9 ribs. InM. septendecim, each tymbal movement produces one simple pulse, an unbroken train of sound waves, not obviously correlated with rib buckling (Fig. 5).5.If, inM. septendecim, the rib buckling frequency determines the fundamental sound frequency, then the latter should increase with rising muscle temperature but this effect is not observed. It is more likely that sound is generated by the tymbal buckling in only 3 or 4 distinct stages, each generating a few oscillations at the fundamental sound frequency. This interpretation is also applicable to the pure-tone song ofChlorocysta viridis.6.It is suggested that pure-tone songs in cicadas are made possible by a reduction in the stiffness of the tymbal. This permits the precise time of buckling of each rib to be influenced by the phase of oscillation in the abdominal resonator, thereby creating a coherent and continuous train of sound waves from one tymbal cycle to another.
Main or calling songs of cicadas Meimuna tavoyana, Platylomia nagarasingna, Platylomia sp. and Purana aff. tigrina from Thailand are described and compared with some previously investigated species. For M. tavoyana a repeated tonal frequency modulated pattern is typical in addition to the broad band buzzing sound. Both closely related chorusing species of Platylomia show broad band acoustic emissions with some degree of frequency band modulation. The song of Purana aff. tigrina from S. Thailand is the most complex, with sharply tuned spectral components (at 2300 and 9400 Hz) and rich amplitude modulation patterns.
Summary 1. Sound output was investigated in males of two cicada species, Cyclochila australasiae Donovan and Macrotristria angularis Stahl. These are large insects, about 4.5 cm in length, with a typical arrangement of sound-producing organs. 2. Songs produced by both species consist of continuous trains of sound pulses, with a fundamental frequency close to 4 kHz. Higher harmonics fall below the 4 kHz peak by 20-30 dB. These songs are the loudest yet recorded among insects: HOdBSPL at 20cm for the protest songs of both species, and values as high as 115 dB for the vigorous calling songs of C. australasiae (mean 113 dB). 3. The male tympanum (ear-drum) is between 3.3 (M. angularis) and 5.5 (C. australasiae) times greater in area than that of the female, which does not sing. The tympana and folded membranes, as well as the sound-generating tymbals, vibrate vigorously during singing; other parts of the insect do not vibrate. 4. Sound output is greatest at the gap between the tympana and their protective coverings, the opercula. High values are also found close to the tymbals but not over the rest of the body. When the gap between tympana and opercula is held closed, rather than open, sound output falls by 11 dB. In the field, calling males adopt a characteristic posture, which keeps this opercular gap wide open. 5. Ablating the tympana makes no difference to the sound output. But ablating the posterior half of the abdominal air sac produces a mean fall of 8.6 dB, together with a great broadening of the song's frequency content. 6. The above results support the conclusion that the majority of sound is radiated through the tympanal opening in typical cicadas, with the tympana being driven passively by the resonant vibrations of air in the air sac. This system can be modelled as a Helmholtz resonator, with the tympanal opening representing the neck of the resonator.
Summary 1. Dried cicada bodies of the species Cyclochila australasiae and model cicadas made from a miniature earphone driving a plastic cavity were used to study the acoustics of sound production in male cicadas. 2. A model cicada with shape and dimensions similar to those of the abdomen of a male C. australasiae resonates at the natural song frequency of the species (4.3 kHz). The abdominal air sac of C. australasiae also resonates at frequencies close to the natural song frequency when excited by external sounds. In an atmosphere of chlorofluorocarbon (CFC) gas, the resonant frequency is lowered in keeping with the decrease in velocity of sound in the CFC gas. 3. At the model's resonant frequency, the driving earphone dissipates more electrical power with the cavity attached than without the cavity. The cavity of the model cicada acts as a narrow-band acoustic acceptance filter, tuned to the natural song frequency. 4. When the miniature earphone emits brief clicks, mimicking those produced by the natural tymbal mechanism, the model cicada produces sound pulses that vary in duration and shape according to the number and timing of the clicks. A coherent train of two or three resonant clicks results in a long slowly-decaying sound pulse similar to that in the natural song. 5. The natural song frequency can be predicted from the dimensions of the abdominal cavity and the tympana in C. australasiae using a simple equation for the resonant frequency of a Helmholtz resonator. This equation also predicts the song frequency of Macrotristria angularis and Magicicada cassini, but it fails with the low-frequency song of Magicicada septendecim. This discrepancy can be accounted for by the unusually thick tympana of M. septendecim, which tend to lower the resonant frequency of the system. 6. We conclude that the abdomen of male cicadas forms a Helmholtz resonator, the components of which are the large air sac as the cavity and the tympana as the neck of the resonator. We suggest that cicada sound production depends on the coupling of two resonators, that of the tymbal and that of the abdominal air sac, from which sound is radiated through the tympana. The coupled resonator system would produce the long sound pulses required for stimulating a sensitive sharply tuned auditory organ.
1. Phonotaxis was investigated in two cicada species: Cystosoma saundersii and Cyclochila australasiae. Females were placed on a stick within a flight cage and presented with artificially generated calling songs. These model calling songs had a range of carrier frequencies, but their temporal parameters were similar to those of the natural calling song. They were broadcast at intensities 30 to 40 dB above the physiological threshold for each frequency.2. Phonotaxis of female Cystosoma saundersii was restricted to a 45 minute period just after sunset, and was highly directional. Between 60 and 70% of flights made during trials in which a model calling song was broadcast were directed towards the loudspeaker at both frequencies tested.3. Phonotaxis of female Cyclochila australasiae occurred throughout the evening, and showed no directional preference toward the loudspeaker. The mean number of flights per trial period was significantly greater in trials during which a model calling song was broadcast than in control trials during which no model calling song was broadcast. There was no significant difference in the mean number of flights per trial with different carrier frequencies.4. In female cicadas, acoustic signals of the males are preferentially graded by the tuned auditory system; phonotactic decisions are then made on the basis of relative intensity without active discrimination between frequencies.
Males of the Palaearctic red cicada, Tibicina haematodes, produce calling songs that are attractive to both sexes. For the first time we (i) describe the organisation of the chorus formed by aggregating males, (ii) analysed the physical characteristics of the calling song, and ( iii) used playback experiments of natural, modified, and allospecific signals to investigate the signal-recognition process. Males overlap each other's calling song and try to call first and last during a chorus, leading to what we term domino and last-word effects, respectively. The calling song consists of a two-part sequence made up of a succession of pulses. It is characterized by slow and fast amplitude modulations and three frequency bands. The structure of the signal varied among individuals in both temporal and frequency parameters. Our playback experiments showed that males make a rough analysis of frequency and duration features of the signal. They pay no attention to amplitude modulations. Because males are not capable of precise analysis, they reply to vari- ous allospecific calling songs. Females' analysis of the calling song being difficult to test, the role of this signal in sex - ual selection still needs to be documented.
The physical characteristics of the free songs of the following seven species of Australian cicadas are analysed: Abricta curvicosta (Germar), Arunta perulata (Guérin), Cystosoma saundersii Westw., Melampsalta (Pauropsalta) encaustica (Germar), Melampsalta (Pauropsalta) mneme (Walk.), Psaltoda harrisii (Leach) and Thopha saccata (F.). Oscillographic Plate I) and sonagraphic (Plates II and III) documentation of this material is provided.
Directional hearing is investigated in males of two species of cicadas, Tympanistalna gastrica (Stål) and Tettigetta josei Boulard, that are similar in size but show different calling song spectra. The vibrational response of the ears is measured with laser vibrometry and compared with thresholds determined from auditory nerve recordings. The data are used to investigate to what extent the directional characteristic of the tympanal vibrations is encoded by the activity of auditory receptors. Laser measurements show complex vibrations of the tympanum, and reveal that directional differences are rather high (>15 dB) in characteristic but limited frequency ranges. At low frequencies, both species show a large directional difference at the same frequency (3–5 kHz) whereas, above 10 kHz, the directional differences correspond to the different resonant frequencies of the respective tymbals. Consequently, due to the mechanical resonance of the tymbal, the frequency range at which directional differences are high differs between the two species that otherwise show similar dimensions of the acoustic system. The directional differences observed in the tympanal vibrations are also observed in the auditory nerve activity. These recordings confirm that the biophysically determined directional differences are available within the nervous system for further processing. Despite considerable intra as well as interindividual variability, the ears of the cicadas investigated here exhibit profound directional characteristics, because the thresholds determined from recordings of the auditory nerve at 30° to the right and left of the longitudinal axis differ by more than 5 dB.
In the locustid Locusta migratoria and the tettigoniids Decticus verrucivorus and Tettigonia cantans, comparative aspects of physiological properties of vibratory/auditory ventral-cord neurones were studied by single cell recordings.These neurones all receive inputs from both vibratory and auditory receptors. Nevertheless, they can be classified into “V neurones” responding preferentially to vibration stimuli, “VS neurones” responding to vibration and airborne sound, and “S neurones” responding preferentially to airborne sound. In every group, there are several types with different physiological properties, normally represented by one neurone on each body side.In Locusta and in the tettigoniid species, the same physiological types of vibratory/auditory neurones were found, although there are differences in the synaptic connectivity of the vibration receptors of the different legs. In Locusta, the middle leg receptors have the strongest influence on the generation of suprathreshold responses of the central neurones, whereas in the tettigoniids the receptors of the ipsilateral fore leg are the most influential.Two of the V neurones receive inputs mainly from campaniform sensilla and other low-frequency vibration receptors, the other V and VS neurones are mainly influenced by the subgenual receptors. Central information processing results in preferential responses to different frequency/intensity ranges in different neurones.Most VS neurone types show the same response characteristics (e.g. time pattern of response, habituation) either to vibration or to airborne-sound stimuli. Simultaneous presentation of both stimuli leads to qualitative changes in the response characteristics. Therefore, the co-processing of auditory and vibratory signals seems to be very important in the acoustic behaviour of grasshoppers.
The responses of single vibratory receptors and ascending ventral cord interneurones were studied extracellularly in Gryllus campestris L. The physiology of the vibration receptors resembled those found in tettigoniids and locusts. The frequency responses of the subgenual receptors provide two possible cues for central frequency discrimination: differences in mean tuning between groups of receptors in the different leg pairs and a range of receptors tuned to different frequencies within one subgenual organ.Most of the ascending vibratory interneurones were highly sensitive in either the low or high frequency range. Broadbanded neurones were less sensitive. The characteristic sensitivity peaks of these units are due mainly to receptor inputs from a particular leg pair, although most central neurones receive inputs from all 6 legs. Only one neurone type, TN1 received excitatory inputs from both auditory and vibratory receptors; its responses were greatly enhanced by the simultaneous presentation of both stimulus modes. The responses to sound stimuli of AN2, on the other hand, were inhibited by vibration. No other auditory interneurones investigated were influenced by inputs from vibration receptors. Central processing of vibratory information in the cricket is compared with that of tettigoniids and locusts.
The calling and courtship songs of 17-year cicadas and of Say's cicadas differ both in the sound frequency spectrum and in temporal pattern. Multiunit recordings with hook electrodes from the whole auditory nerve show that the hearing organs are especially sensitive to transient stimuli occurring in natural sounds. Artificially produced clicks elicit bursts of spikes synchronized among various primary sensory fibres. These fibres respond to natural calling and courtship songs with a specificity dependent on carrier frequency, rhythm and transient content of the sound, following sound pulses (i.e. tymbal actions) up to repetition rates of 200 Hz. An ascending, plurisegmental interneurone was characterized by intracellular recording and simultaneously stained with cobalt. Its main arborization spatially overlaps the anterior part of the sensory auditory neuropile, and the axon was traced as far as the prothoracic ganglion. Direct input from primary auditory fibres was suggested by latency measurements. Intracellular recordings from such neurons in different species show distinct auditory input, with phasic-tonic spike responses to tones. In general, the interneurone response is more species-specific to calling than to courtship songs, and the preferential response to the conspecific calling song is based primarily upon sound frequency content.
To estimate the potential contribution of ethological and ecological parameters to the mechanisms of species formation and species isolation in the Palearctic cicada genus Tibicina, we constructed a molecular phylogenetic hypothesis of extant Tibicina species. Seven mitochondrial genes and a fragment of a nuclear gene were sequenced (3046 bp). Mitochondrial genes included 547 informative sites but the nuclear gene was too conserved to be included in the analysis. The tree was characterized by a basal polytomy indicating that Tibicina species arose rapidly. Such rapid radiation might explain the low divergence in the acoustic communication observed between species. Parameters describing habitat selection and acoustic communication were mapped onto the tree. A shift in habitat selection accompanied by acoustic changes might have contributed to one speciation event. The stochastic distribution of the same acoustic characters on the other branches of the tree implies, however, that the subtle acoustic differences between species could be the result of previous speciation events and independent evolutionary histories, rather than having contributed themselves in the speciation and isolation processes. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91, 611–626.
Males of Tibicina cicada species produce a sustained and monotonous calling song by tymbal activity. This acoustic signal constitutes the first step in pair formation, attracting females at long range, and is involved in male–male interactions. The specificity of this signal was investigated for the first time for seven species and one subspecies of Tibicina occurring in France. This analysis was achieved by describing tymbal anatomy, tymbal mechanism and calling song structure. Male calling songs are emitted following the same general scheme: tymbals are activated alternately and the successive buckling of the sclerotized ribs that they bear produces a regular succession of groups of pulses. The structural and mechanical properties shared by Tibicina species and subspecies lead to a considerable uniformity of the signal shape. Nevertheless, a principal component analysis applied to eight temporal and three frequency parameters revealed differences between the signals of the species studied. In particular, calling songs differed in groups of pulse rate and/or in peak of the second frequency band (carrier frequency). These acoustic differences are probably linked to differences in the numbers of tymbal ribs and body size. Groups of pulse rate and/or peak of the second frequency band could encode specific information. However, Tibicina calling songs may not act as distinct specific-mate recognition systems and may not play a leading role in the mating isolation process; rather, they might merely belong to a complex set of specific spatial, ecological, ethological and morphological characters that ensure syngamy.