Cicada Acoustic Communication

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.

[1]  Moulds Song analyses of cicadas of the genera Aleeta Moulds and Tryella Moulds (Hemiptera: Cicadidae) , 2005 .

[2]  D. Young,et al.  ANALYSIS OF SONGS OF SOME AUSTRALIAN CICADAS (HOMOPTERA: CICADIDAE) , 1972 .

[3]  D. Young,et al.  PHONOTAXIS IN THE CICADAS CYSTOSOMA SAUNDERSII AND CYCLOCHILA AUSTRALASIAE , 1997 .

[4]  Matija Gogala,et al.  SONGS OF FOUR CICADA SPECIES FROM THAILAND , 1995 .

[5]  Paulo J. Fonseca,et al.  Asymmetry of tymbal action and structure in a cicada: a possible role in the production of complex songs , 1998, The Journal of experimental biology.

[6]  Axel Michelsen,et al.  Tuned directionality in cricket ears , 1995, Nature.

[7]  Axel Michelsen,et al.  Time Resolution in Auditory Systems , 1985, Proceedings in Life Sciences.

[8]  Roland Kühne Neurophysiology of the vibration sense in locusts and bushcrickets: The responses of ventral-cord neurones , 1982 .

[9]  Franz Huber,et al.  Sound production in periodical cicadas (Homoptera: Cicadidae: Magicicada septendecim, M. cassini) , 1987 .

[10]  José A. Quartau,et al.  Selective Responsiveness in Males of Cicada orni to Conspecific and Allospecific Calling Songs (Hemiptera: Cicadidae) , 2006 .

[11]  Daniel Robert,et al.  Tuning the drum: the mechanical basis for frequency discrimination in a Mediterranean cicada , 2006, Journal of Experimental Biology.

[12]  Andrej V. Popov Co-Evolution of Sound-Production and Hearing in Insects , 1990 .

[13]  Axel Michelsen,et al.  Pressure difference receiving ears , 2008, Bioinspiration & biomimetics.

[14]  Thierry Aubin,et al.  Acoustic communication in the Palaearctic red cicada, Tibicina haematodes: chorus organisation, calling-song structure, and signal recognition , 2002 .

[15]  Jérôme Sueur,et al.  Cicadas from Portugal: revised list of species with eco-ethological data (Hemiptera: Cicadidae) , 2004 .

[16]  C. Simon,et al.  Steady Plio-Pleistocene diversification and a 2-million-year sympatry threshold in a New Zealand cicada radiation. , 2008, Molecular phylogenetics and evolution.

[17]  B. Ronacher,et al.  Temperature dependence of temporal resolution in an insect nervous system , 2002, Journal of Comparative Physiology A.

[18]  P. Fonseca,et al.  Directional hearing of a cicada: biophysical aspects , 1993, Journal of Comparative Physiology A.

[19]  Ronald R. Hoy,et al.  Comparative Hearing: Insects , 1998, Springer Handbook of Auditory Research.

[20]  J. Pringle,et al.  A Physiological Analysis of Cicada Song , 1954 .

[21]  P. Fonseca,et al.  Song discrimination by male cicadas Cicada barbara lusitanica (Homoptera, Cicadidae). , 2002, The Journal of experimental biology.

[22]  P. Dallos The active cochlea , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  Peter J. Simmons,et al.  The Tymbal Mechanism and Song Patterns of the Bladder Cicada, Cystosoma Saundersii , 1978 .

[24]  Franz Huber,et al.  Auditory nerve and interneurone responses to natural sounds in several species of cicadas , 1980 .

[25]  J. Cooley,et al.  Sexual behavior in North American cicadas of the genera Magicicada and Okanagana. , 1999 .

[26]  Andrew C. Mason,et al.  Hearing in a primitive ensiferan: the auditory system of Cyphoderris monstrosa (Orthoptera: Haglidae) , 1991, Journal of Comparative Physiology A.

[27]  A. V. Popov Sound production and hearing in the cicada,Cicadetta sinuatipennis osh. (Homoptera, Cicadidae) , 2004, Journal of comparative physiology.

[28]  Susan Silver,et al.  Processing of vibratory and acoustic signals by ventral cord neurones in the cricket Gryllus campestris , 1984 .

[29]  A. V. Popov,et al.  Sound radiation in a cicada: the role of different structures , 1994, Journal of Comparative Physiology A.

[30]  K. G. Hill,et al.  Structure and function of the auditory system of the cicada,Cystosoma saundersii , 2004, Journal of comparative physiology.

[31]  O. Hendrich,et al.  Power gain exhibited by motile mechanosensory neurons in Drosophila ears. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[32]  David M. Lambert,et al.  Speciation and the recognition concept : theory and application , 1995 .

[33]  K. G. Pearson,et al.  A preparation for the intracellular analysis of neuronal activity during flight in the locust , 1982, Journal of comparative physiology.

[34]  B. Hedwig A descending brain neuron elicits stridulation in the cricketGryllus bimaculatus (de Geer) , 2005, Naturwissenschaften.

[35]  Peggy S. M. Hill,et al.  Vibration and Animal Communication: A Review1 , 2001 .

[36]  Maurice J. Kernan Mechanotransduction and auditory transduction in Drosophila , 2007, Pflügers Archiv - European Journal of Physiology.

[37]  Thierry Aubin,et al.  Specificity of cicada calling songs in the genus Tibicina (Hemiptera: Cicadidae) , 2003 .

[38]  R. Fettiplace Electrical tuning of hair cells in the inner ear , 1987, Trends in Neurosciences.

[39]  Hennig,et al.  Phasic action of the tensor muscle modulates the calling song in cicadas , 1996, The Journal of experimental biology.

[40]  Paulo J. Fonseca,et al.  Sound production in cicadas: timbal muscle activity during calling song and protest song , 1996 .

[41]  J. Tougaard,et al.  Energy detection and temporal integration in the noctuid A1 auditory receptor , 1996, Journal of Comparative Physiology A.

[42]  D. Marshall,et al.  REPRODUCTIVE CHARACTER DISPLACEMENT AND SPECIATION IN PERIODICAL CICADAS, WITH DESCRIPTION OF A NEW SPECIES, 13‐YEAR MAGICICADA NEOTREDECIM , 2000, Evolution; international journal of organic evolution.

[43]  P J Fonseca,et al.  Effects of temperature on tuning of the auditory pathway in the cicada Tettigetta josei (Hemiptera, Tibicinidae) , 2007, Journal of Experimental Biology.

[44]  G Matija,et al.  FAUNA OF SINGING CICADAS (AUCHENORRHYNCHA: CICADOIDEA) OF MACEDONIA - A BIOACOUSTIC SURVEY , 2005 .

[45]  H. Kleindienst,et al.  The role of the medial septum in the acoustic trachea of the cricket Gryllus bimaculatus , 1994, Journal of Comparative Physiology A.

[46]  David C. Young,et al.  Do Cicadas Radiate Sound through their Ear-Drums? , 1990 .

[47]  Hennig,et al.  AUDITORY THRESHOLD CHANGE IN SINGING CICADAS , 1994, The Journal of experimental biology.

[48]  P. Fonseca,et al.  Temperature dependence of cicada songs (Homoptera, Cicadoidea) , 2002, Journal of Comparative Physiology A.

[49]  D. Young,et al.  Neuromuscular mechanism of sound production in Australian cicadas , 1972, Journal of comparative physiology.

[50]  B Hedwig,et al.  Control of cricket stridulation by a command neuron: efficacy depends on the behavioral state. , 2000, Journal of neurophysiology.

[51]  D. Young,et al.  Mechanisms of sound-production and muscle contraction kinetics in cicadas , 1983, Journal of comparative physiology.

[52]  John R. Cooley,et al.  SEXUAL SIGNALING IN PERIODICAL CICADAS, MAGICICADA SPP. (HEMIPTERA: CICADIDAE) , 2001 .

[53]  Bennet-Clark Tymbal mechanics and the control of song frequency in the cicada Cyclochila australasiae , 1997, The Journal of experimental biology.

[54]  F. Huber,et al.  Central projections of fibers in the auditory and tensor nerves of cicadas (Homoptera: Cicadidae) , 2004, Cell and Tissue Research.

[55]  Franz Huber,et al.  Acoustic Communication in Periodical Cicadas: Neuronal Responses to Songs of Sympatric Species , 1990 .

[56]  R M Hennig,et al.  Auditory perception: How cicadas interpret acoustic signals , 2000, Nature.

[57]  Thomas E. Moore,et al.  Substrate vibrations during acoustic signalling in the cicada Okanagana rimosa , 2002, Journal of insect science.

[58]  Bennet-Clark Sound radiation by the bladder cicada cystosoma saundersii , 1998, The Journal of experimental biology.

[59]  A. V. Popov,et al.  Directionality of the tympanal vibrations in a cicada: a biophysical analysis , 1997, Journal of Comparative Physiology A.

[60]  Bennet-Clark,et al.  The role of the tymbal in cicada sound production , 1995, The Journal of experimental biology.

[61]  B. Ronacher,et al.  Temporal modulation transfer functions in auditory receptor fibres of the locust (Locusta migratoria L.) , 2002, Journal of Comparative Physiology A.

[62]  D. Young,et al.  Pure-tone songs in cicadas with special reference to the genusMagicicada , 1983, Journal of comparative physiology.

[63]  Daniel Robert,et al.  Sexual dimorphism in auditory mechanics: tympanal vibrations of Cicada orni , 2008, Journal of Experimental Biology.

[64]  Ville de Longueuil,et al.  CONTRIBUTION TO THE KNOWLEDGE OF THE SINGING CICADAS (AUCHENORRHYNCHA: CICADOIDEA) OF ROMANIA , 2006 .

[65]  Paulo J. Fonseca,et al.  CHARACTERISTICS OF THE ACOUSTIC SIGNALS IN NINE SPECIES OF CICADAS (HOMOPTERA, CICADIDAE) , 1991 .

[66]  Daniel Robert,et al.  Active auditory mechanics in mosquitoes , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[67]  R. Josephson,et al.  A Synchronous Insect Muscle with an Operating Frequency Greater than 500 Hz , 1985 .

[68]  D. Young,et al.  The Organization of the Auditory Organ of the Bladder Cicada, Cystosoma Saundersii , 1981 .

[69]  R. H. Wiley,et al.  Reverberations and Amplitude Fluctuations in the Propagation of Sound in a Forest: Implications for Animal Communication , 1980, The American Naturalist.

[70]  J. Bacon,et al.  Sexual dimorphism of motorneurons: Timbal muscle innervation in male periodical cicadas and homologous structures in females , 2004, Cell and Tissue Research.

[71]  Jérôme Sueur,et al.  Molecular phylogeny of the genus Tibicina (Hemiptera, Cicadidae): rapid radiation and acoustic behaviour , 2007 .

[72]  P. Simmons,et al.  Neuronal generation of singing in a cicada , 1977, Nature.

[73]  J. Cooley,et al.  Long-range Acoustical Signals, Phonotaxis, and Risk in the Sexual Pair-Forming Behaviors of Okanagana canadensis and O. rimosa (Hemiptera: Cicadidae) , 2001 .

[74]  H C Bennet-Clark,et al.  Resonators in insect sound production: how insects produce loud pure-tone songs. , 1999, The Journal of experimental biology.

[75]  R. Josephson,et al.  Power and control muscles of cicada song: structural and contractile heterogeneity , 2004, Journal of Comparative Physiology A.

[76]  John MacDonald,et al.  Australian cicadas [Book Review] , 1990 .

[77]  Richard Vogel Tübingen Über ein tympanales Sinnesorgan, das mutmaßliche Hörorgan der Singzikaden , 2007, Zeitschrift für Anatomie und Entwicklungsgeschichte.

[78]  D. Young,et al.  Relative Importance of Song Parameters During Flight Phonotaxis and Courtship in the Bladder Cicada Cystosoma Saundersii , 1989 .

[79]  Bernhard Ronacher,et al.  Filtering of behaviourally relevant temporal parameters of a grasshopper's song by an auditory interneuron , 1988, Journal of Comparative Physiology A.

[80]  J. Tougaard,et al.  Detection of short pure-tone stimuli in the noctuid ear: what are temporal integration and integration time all about? , 1998, Journal of Comparative Physiology A.

[81]  S. Hagiwara,et al.  Discharges in motoneurons of cicada. , 1956, Journal of cellular and comparative physiology.

[82]  Daniel Robert,et al.  Sound emission and reception tuning in three cicada species sharing the same habitat. , 2010, The Journal of the Acoustical Society of America.

[83]  K. G. Pearson,et al.  Interneuronal organization in the flight system of the locust , 1984 .

[84]  Axel Michelsen,et al.  Biophysics of Sound Localization in Insects , 1998 .

[85]  Paulo J. Fonseca,et al.  Directional characteristics of the auditory system of cicadas: is the sound producing tymbal an integral part of directional hearing? , 2004 .

[86]  D. Gwynne,et al.  Sex-biased predation and the risky mate-locating behaviour of male tick-tock cicadas (Homoptera: Cicadidae) , 1987, Animal Behaviour.

[87]  Paulo J. Fonseca,et al.  THE EVOLUTION OF CICADA SONGS CONTRASTED WITH THE RELATIONSHIPS INFERRED FROM MITOCHONDRIAL DNA (INSECTA, HEMIPTERA) , 2008 .

[88]  H. C. Bennet-Clark,et al.  A MODEL OF THE MECHANISM OF SOUND PRODUCTION IN CICADAS , 1992 .

[89]  R. Fettiplace,et al.  Force generation by mammalian hair bundles supports a role in cochlear amplification , 2005, Nature.

[90]  G. Wendler,et al.  The role of the medial septum in the acoustic trachea of the cricket Gryllus bimaculatus , 1993, Journal of Comparative Physiology A.