The sounds of silence: cessation of singing and song pausing are ultrasound-induced acoustic startle behaviors in the katydid Neoconocephalus ensiger (Orthoptera; Tettigoniidae)

Abstract Previous studies of acoustic startle in insects have dealt with behavioral and/or neural mechanisms employed in evading aerially hawking, echolocating bats; however, insects also face terrestrial predators. Here we describe an acoustic startle response of the nocturnal katydid, Neoconocephalus ensiger. Stridulating males disturbed in the field perform obvious anti-predatory behaviors – cessation of singing, freezing, jumping, and evasive flight. Under controlled laboratory conditions we found that cessation of singing and song pausing are ultrasound-specific behaviors: when stimulated with pulsed ultrasound (20–100 kHz), but not audio-sound (<20 kHz), males cease mate calling or insert pauses in their song. A second factor influencing acoustic startle is the phase of stimulation: an acoustic startle response occurs only when the pulse of ultrasound arrives during the window of silence between stridulatory syllables. The average startle threshold and response latency was 70 ± 5 dB SPL and 34.2 ± 6.0 ms, respectively. N. ensiger is particularly useful for examining acoustic startle responses of non-flying insects because (1) its calling song is broadband and contains ultrasound, thus the possibility exists of confusion over the biological meaning of ultrasound, and (2) this species shows the classic bat-avoidance response while flying, so a direct comparison between two types of acoustic startle is possible within the same species.

[1]  H. Y. Elder HIGH FREQUENCY MUSCLES USED IN SOUND PRODUCTION BY A KATYDID. II. ULTRASTRUCTURE OF THE SINGING MUSCLES , 1971 .

[2]  M. Ritchie The Tettigoniidae. Biology, Systematics and Evolution, W.J. Bailey, D.C.F. Rentz (Eds.). Springer-Verlag, Berlin (1990), xi , 1992 .

[3]  R. Hoy,et al.  The neurobiology of cricket song. , 1974, Scientific American.

[4]  K. D. Roeder MOTHS AND ULTRASOUND. , 1965, Scientific American.

[5]  D. D. Yager,et al.  Behavioral response to ultrasound by the tiger beetle Cicindela marutha dow combines aerodynamic changes and sound production. , 1997, The Journal of experimental biology.

[6]  T. J. Walker Experimental Demonstration of a Cat Locating Orthopteran Prey by the Prey's Calling Song , 1964 .

[7]  Michael D Greenfield Evolution of Acoustic Communication in the Genus Neoconocephalus: Discontinuous Songs, Synchrony, and Interspecific Interactions , 1990 .

[8]  D. Gwynne MATING BEHAVIOR OF NEOCONOCEPHALUS ENSIGER (ORTHOPTERA: TETTIGONIIDAE) WITH NOTES ON THE CALLING SONG , 1977, The Canadian Entomologist.

[9]  E. Sismondo,et al.  Synchronous, Alternating, and Phase-Locked Stridulation by a Tropical Katydid , 1990, Science.

[10]  J. E. Heath,et al.  BODY TEMPERATURE AND SINGING IN THE KATYDID, NEOCONOCEPHALUS ROBUSTUS (ORTHOPTERA, TETTIGONIIDAE) , 1970 .

[11]  R. Hoy The Evolution of Hearing in Insects as an Adaptation to Predation from Bats , 1992 .

[12]  K. D. Roeder Turning tendency of moths exposed to ultrasound while in stationary flight , 1967 .

[13]  Andrew C. Mason,et al.  High ultrasonic and tremulation signals in neotropical katydids (Orthoptera: Tettigoniidae) , 1994 .

[14]  J. Schul Neuronal basis of phonotactic behaviour in Tettigonia viridissima : processing of behaviourally relevant signals by auditory afferents and thoracic interneurons , 1997, Journal of Comparative Physiology A.

[15]  T. Bullock Comparative Neuroethology of Startle, Rapid Escape, and Giant Fiber-Mediated Responses , 1984 .

[16]  Silence as a Defense against Predatory Bats in Two Species of Calling Insects , 1984 .

[17]  R. Hoy Startle, categorical response, and attention in acoustic behavior of insects. , 1989, Annual review of neuroscience.

[18]  Keir G. Pearson,et al.  Escape Behavior of the Locust , 1984 .

[19]  G. K. Morris,et al.  Bat Predation and Its Influence on Calling Behavior in Neotropical Katydids , 1987, Science.

[20]  T. J. Walker Stridulatory movements in eight species of Neoconocephalus (Tettigoniidae). , 1975, Journal of insect physiology.

[21]  T W Picton,et al.  Normal hearing thresholds for clicks. , 1982, The Journal of the Acoustical Society of America.

[22]  T. G. Forrest,et al.  Ultrasound acoustic startle response in scarab beetles. , 1995, The Journal of experimental biology.

[23]  The Effect of Acoustic Signals on the Chirp Rhythm in the Bush Cricket Pholidoptera Griseoaptera , 1974 .

[24]  Responses of nonflying moths to ultrasound: the threat of gleaning bats , 1981 .

[25]  G. Sales,et al.  Ultrasonic Communication by Animals , 1974 .

[26]  K. D. Roeder,et al.  The detection and evasion of bats by moths , 1961 .

[27]  D. Robert,et al.  Tympanal hearing in insects. , 1996, Annual review of entomology.

[28]  R. Josephson,et al.  HIGH FREQUENCY MUSCLES USED IN SOUND PRODUCTION BY A KATYDID. I. ORGANIZATION OF THE MOTOR SYSTEM , 1971 .

[29]  L. Miller The behaviour of flying green lacewings, Chrysopa carnea, in the presence of ultrasound , 1975 .

[30]  Michael D Greenfield,et al.  Synchronous and Alternating Choruses in Insects and Anurans: Common Mechanisms and Diverse Functions , 1994 .

[31]  J. Castner,et al.  Strategies Utilized by Katydids (Orthoptera: Tettigoniidae) against Diurnal Predators in Rainforests of Northeastern Peru , 1995 .

[32]  J. H. Zar,et al.  Biostatistical Analysis (5th Edition) , 1984 .

[33]  K. C. Shaw An Analysis of the Phonoresponse of Males of the True Katydid, Pterophylla Camellifolia (Fabricius) (Orthoptera: Tettigoniidae) , 1968 .

[34]  S. Counter Bioacoustics and neurobiology of communication in the tettigoniid Neoconocephalus robustus. , 1977, Journal of insect physiology.

[35]  T. J. Walker,et al.  Acoustic Synchrony: Two Mechanisms in the Snowy Tree Cricket , 1969, Science.

[36]  K. Schäfer,et al.  Oscillation and noise determine signal transduction in shark multimodal sensory cells , 1994, Nature.

[37]  J. McNeil,et al.  Predation risk and mating behavior: the responses of moths to bat-like ultrasound , 1998 .

[38]  J. W. Dawson,et al.  The gleaning attacks of the northern long-eared bat, Myotis septentrionalis, are relatively inaudible to moths. , 1993, The Journal of experimental biology.

[39]  Jacqueline J. Belwood,et al.  Anti-Predator Defences and Ecology of Neotropical Forest Katydids, Especially the Pseudophyllinae , 1990 .

[40]  M. D. Jones The acoustic behaviour of the bush cricket Pholidoptera griseoaptera. 2. Interaction with artificial sound signals. , 1966, The Journal of experimental biology.

[41]  M. D. Jones The acoustic behaviour of the bush cricket Pholidoptera griseoaptera. I. Alternation, synchronism and rivalry between males. , 1966, The Journal of experimental biology.

[42]  D. Robert THE AUDITORY BEHAVIOUR OF FLYING LOCUSTS , 1989 .

[43]  Michael D Greenfield,et al.  Katydid synchronous chorusing is an evolutionarily stable outcome of female choice , 1993, Nature.

[44]  I. J. Cantrall The ecology of the Orthoptera and Dermaptera of the George Reserve, Michigan. , 1943 .

[45]  K. D. Roeder,et al.  Nerve Cells and Insect Behavior , 1998 .

[46]  P. Brodfuehrer,et al.  The neuroethology of acoustic startle and escape in flying insects. , 1989, The Journal of experimental biology.

[47]  M. Fenton,et al.  Ultrasound-triggered, flight-gated evasive maneuvers in the praying mantis Parasphendale agrionina. I. Free flight. , 1990, The Journal of experimental biology.