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Gleaning bat echolocation calls do not elicit antipredator behaviour in the Pacific field cricket, Teleogryllus oceanicus (Orthoptera: Gryllidae)

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Abstract

Bats that glean prey (capture them from surfaces) produce relatively inconspicuous echolocation calls compared to aerially foraging bats and could therefore be difficult predators to detect, even for insects with ultrasound sensitive ears. In the cricket Teleogryllus oceanicus, an auditory interneuron (AN2) responsive to ultrasound is known to elicit turning behaviour, but only when the cricket is in flight. Turning would not save a cricket from a gleaning bat so we tested the hypothesis that AN2 elicits more appropriate antipredator behaviours when crickets are on the ground. The echolocation calls of Nyctophilus geoffroyi, a sympatric gleaning bat, were broadcast to singing male and walking female T. oceanicus. Males did not cease singing and females did not pause walking more than usual in response to the bat calls up to intensities of 82 dB peSPL. Extracellular recordings from the cervical connective revealed that the echolocation calls elicited AN2 action potentials at high firing rates, indicating that the crickets could hear these stimuli. AN2 appears to elicit antipredator behaviour only in flight, and we discuss possible reasons for this context-dependent function.

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Abbreviations

AN2:

Ascending neuron 2

ASR:

Acoustic startle response

References

  • Anderson ME, Racey PA (1993) Discrimination between fluttering and non-fluttering moths by brown long-eared bats, Plecotus auritus. Anim Behav 46:1151–1155

    Article  Google Scholar 

  • Bailey WJ, Haythornthwaite S (1998) Risks of calling by the field cricket Teleogryllus oceanicus; potential predation by Australian long-eared bats. J Zool, Lond 244:505–513

    Article  Google Scholar 

  • Bailey WJ, Thomson P (1977) Acoustic orientation in the cricket Teleogryllus oceanicus (Le Guillou). J Exp Biol 67:61–75

    Google Scholar 

  • Bailey NW, McNabb JR, Zuk M (2008) Preexisting behavior facilitated the loss of a sexual signal in the field cricket Teleogryllus oceanicus. Behav Ecol 19:202–207

    Article  Google Scholar 

  • Bell GP (1982) Behavioral and ecological aspects of gleaning by a desert insectivorous bat, Antrozous pallidus (Chiroptera: Vespertilionidae). Behav Ecol Sociobiol 10:217–223

    Article  Google Scholar 

  • Belwood JJ, Morris GK (1987) Bat predation and its influence on calling behavior in Neotropical katydids. Science 238:64–67

    Article  PubMed  Google Scholar 

  • Casaday GB, Hoy RR (1977) Auditory interneurons in the cricket Teleogryllus oceanicus: physiological and anatomical properties. J Comp Physiol 121:1–13

    Article  Google Scholar 

  • Faulkes Z, Pollack GS (2000) Effects of inhibitory timing on contrast enhancement in auditory circuits in crickets (Teleogryllus oceanicus). J Neurophysiol 84:1247–1255

    PubMed  CAS  Google Scholar 

  • Faure PA, Barclay RMR (1992) The sensory basis of prey detection by the long-eared bat, Myotis evotis, and the consequences for prey selection. Anim Behav 44:31–39

    Article  Google Scholar 

  • Faure PA, Barclay RMR (1994) Substrate-gleaning versus aerial-hawking: plasticity in the foraging and echolocation behaviour of the long-eared bat, Myotis evotis. J Comp Physiol A 174:651–660

    Article  PubMed  CAS  Google Scholar 

  • Faure PA, Hoy RR (2000a) The sounds of silence: cessation of singing and song pausing are ultrasound-induced acoustic startle behaviors in the katydid Neoconocephalus ensiger (Orthoptera; Tettigoniidae). J Comp Physiol A 186:129–142

    Article  PubMed  CAS  Google Scholar 

  • Faure PA, Hoy RR (2000b) Neuroethology of the katydid T-cell. I. Tuning and responses to pure tones. J Exp Biol 203:3225–3242

    PubMed  CAS  Google Scholar 

  • Faure PA, Fullard JH, Dawson JW (1993) The gleaning attacks of the Northern long-eared bat, Myotis septentrionalis, are relatively inaudible to moths. J Exp Biol 178:173–189

    PubMed  CAS  Google Scholar 

  • Fenton MB, Gaudet CL, Leonard ML (1983) Feeding behaviour of the bats Nycteris grandis and Nycteris thebaica (Nycteridae) in captivity. J Zool, Lond 200:347–354

    Article  Google Scholar 

  • Findley JS (1993) Bats: a community perspective. Cambridge University Press, Cambridge

    Google Scholar 

  • Forrest TG, Lajoie DR, Cusick D (2006) Calling songs, duets, and auditory tuning in two cryptic katydids (Tettigoniidae: Phaneropterinae: Amblycorypha). Ann Entomol Soc Am 99:978–987

    Article  Google Scholar 

  • Fullard JH, Koehler C, Surlykke A, McKenzie NL (1991) Echolocation ecology and flight morphology of insectivorous bats (Chiroptera) in South-western Australia. Aus J Zool 39:427–438

    Article  Google Scholar 

  • Fullard JH, Ratcliffe JM, Guignion C (2005) Sensory ecology of predator-prey interactions: responses of the AN2 interneuron in the field cricket Teleogryllus oceanicus to the echolocation calls of sympatric bats. J Comp Physiol A 191:605–618

    Article  Google Scholar 

  • Fuzessery ZM, Buttenhoff P, Andrews B, Kennedy JM (1993) Passive sound localization of prey by the pallid bat (Antrozous p. pallidus). J Comp Physiol A 171:767–777

    Article  PubMed  CAS  Google Scholar 

  • Grant JDA (1991) Prey location by two Australian long-eared bats, Nyctophilus gouldi and N. geoffroyi. Aust J Zool 39:45–56

    Article  Google Scholar 

  • Harrison L, Horseman G, Lewis B (1988) The coding of the courtship song by an identified auditory neurone in the cricket Teleogryllus oceanicus (Le Guillou). J Comp Physiol A 163:215–225

    Article  Google Scholar 

  • Hedrick AV, Dill LM (1993) Mate choice by female crickets is influenced by predation risk. Anim Behav 46:193–196

    Article  Google Scholar 

  • Hedrick AV, Kortet R (2006) Hiding behaviour in two cricket populations that differ in predation pressure. Anim Behav 72:1111–1118

    Article  Google Scholar 

  • Hosken DJ, Bailey WJ, O’Shea JE, Roberts JD (1994) Localisation of insect calls by the bat Nyctophilus geoffroyi (Chiroptera: Vespertilionidae): a laboratory study. Aus J Zool 42:177–184

    Article  Google Scholar 

  • Hoy RR (1991) Signals for survival in the lives of crickets. Am Zool 31:297–305

    Google Scholar 

  • Hoy RR, Nolen T, Brodfuehrer P (1989) The neuroethology of acoustic startle and escape in flying insects. J Exp Biol 146:287–306

    PubMed  CAS  Google Scholar 

  • Hutchings M, Lewis B (1984) The role of two-tone suppression in song coding by ventral cord neurones in the cricket Teleogryllus oceanicus (Le Guillou). J Comp Physiol A 154:103–112

    Article  Google Scholar 

  • Latimer W, Lewis DB (1986) Song harmonic content as a parameter determining acoustic orientation behaviour in the cricket Teleogryllus oceanicus (Le Guillou). J Comp Physiol A 158:583–591

    Article  Google Scholar 

  • Libersat F, Hoy RR (1991) Ultrasonic startle behavior in bushcrickets (Orthoptera; Tettigoniidae). J Comp Physiol A 169:507–514

    Article  PubMed  CAS  Google Scholar 

  • Miller LA, Treat AE (1993) Field recordings of echolocation and social signals from the gleaning bat Myotis septentrionalis. Bioacoustics 5:67–87

    Google Scholar 

  • Moiseff A, Hoy RR (1983) Sensitivity to ultrasound in an identified auditory interneuron in the cricket: a possible neural link to phonotactic behavior. J Comp Physiol 152:155–167

    Article  Google Scholar 

  • Moiseff A, Pollack GS, Hoy RR (1978) Steering responses of flying crickets to sound and ultrasound: mate attraction and predator avoidance. Proc Natl Acad Sci USA 75:4052–4056

    Article  PubMed  Google Scholar 

  • Nabatiyan A, Poulet JFA, de Polavieja GG, Hedwig B (2003) Temporal pattern recognition based on instantaneous spike rate coding in a simple auditory system. J Neurophysiol 90:2484–2493

    Article  PubMed  CAS  Google Scholar 

  • Neuweiler G (1989) Foraging ecology and audition in echolocating bats. Trends Ecol Evol 4:160–166

    Article  Google Scholar 

  • Nolen TG, Hoy RR (1984) Initiation of behavior by single neurons: the role of behavioural context. Science 226:992–994

    Article  PubMed  CAS  Google Scholar 

  • Nolen TG, Hoy RR (1986) Phonotaxis in flying crickets. II. Physiological mechanisms of two-tone suppression of the high frequency avoidance steering behavior by the calling song. J Comp Physiol A 159:441–456

    Article  PubMed  CAS  Google Scholar 

  • Nolen TG, Hoy RR (1987) Postsynaptic inhibition mediates high-frequency selectivity in the cricket Teleogryllus oceanicus: implications for flight phonotaxis behavior. J Neurosci 7:2081–2096

    PubMed  CAS  Google Scholar 

  • Oldfield BP (1980) Accuracy of orientation in female crickets, Teleogryllus oceanicus (Gryllidae): dependence on song spectrum. J Comp Physiol 141:93–99

    Article  Google Scholar 

  • Otte D (1992) Evolution of cricket songs. J Orthop Res 1:25–49

    Google Scholar 

  • Pavey CR, Burwell CJ, Milne DJ (2006) The relationship between echolocation-call frequency and moth predation of a tropical bat fauna. Can J Zool 84:425–433

    Article  Google Scholar 

  • Pollack GS (1998) Neural processing of acoustic signals. In: Hoy RR, Popper AN, Fay RR (eds) Comparative hearing: insects. Springer, New York, pp 139–196

    Google Scholar 

  • Pollack GS, Martins R (2007) Flight and hearing: ultrasound sensitivity differs between flight-capable and flight-incapable morphs of a wing-dimorphic cricket species. J Exp Biol 210:3160–3164

    Article  PubMed  Google Scholar 

  • Pollack GS, Huber F, Weber T (1984) Frequency and temporal pattern-dependent phonotaxis of crickets (Teleogryllus oceanicus) during tethered flight and compensated walking. J Comp Physiol A 154:13–26

    Article  Google Scholar 

  • Poulet JFA, Hedwig B (2002) A corollary discharge maintains auditory sensitivity during sound production. Nature 418:872–876

    Article  PubMed  CAS  Google Scholar 

  • Poulet JFA, Hedwig B (2003) Corollary discharge inhibition of ascending auditory neurons in the stridulating cricket. J Neurosci 23:4717–4725

    PubMed  CAS  Google Scholar 

  • Ratcliffe JM, Fenton MB, Shettleworth SJ (2006) Behavioral flexibility positively correlated with relative brain volume in predatory bats. Brain Behav Evol 67:165–176

    Article  PubMed  Google Scholar 

  • Ritzmann RE, Tobias ML, Fourtner CR (1980) Flight activity initiated by giant interneurons of the cockroach: evidence for bifunctional trigger interneurons. Science 210:443–445

    Article  PubMed  Google Scholar 

  • Schildberger K, Hörner M (1988) The function of auditory neurons in cricket phonotaxis. I. Influence of hyperpolarization of identified neurons on sound localization. J Comp Physiol A 163:621–631

    Article  Google Scholar 

  • Schul J (1997) Neuronal basis of phonotactic behaviour in Tettigonia viridissima: processing of behaviourally relevant signals by auditory afferents and thoracic interneurons. J Comp Physiol A 180:573–583

    Article  Google Scholar 

  • Schul J, Schulze W (2001) Phonotaxis during walking and flight: are differences in selectivity due to predation pressure? Naturwissenschaften 88:428–442

    Article  CAS  Google Scholar 

  • Schulze W, Schul J (2001) Ultrasound avoidance behaviour in the bushcricket Tettigonia viridissima (Orthoptera: Tettigoniidae). J Exp Biol 204:733–740

    PubMed  CAS  Google Scholar 

  • Stapells DR, Picton TW, Smith AD (1982) Normal hearing thresholds for clicks. J Acoust Soc Am 72:74–79

    Article  PubMed  CAS  Google Scholar 

  • Suga N (1966) Ultrasonic production and its reception in some Neotropical Tettigoniidae. J Insect Physiol 12:1039–1050

    Article  PubMed  CAS  Google Scholar 

  • ter Hofstede HM, Fullard JH (2008) The neuroethology of song cessation in response to gleaning bat calls in two species of katydids, Neoconocephalus ensiger and Amblycorypha oblongifolia. J Exp Biol 211:2431–2441

    Article  PubMed  Google Scholar 

  • Tuttle MD, Ryan MJ, Belwood JJ (1985) Acoustical resource partitioning by two species of Phyllostomid bats (Trachops cirrhosus and Tonatia sylvicola). Anim Behav 33:1369–1371

    Article  Google Scholar 

  • Van Dyck S, Strahan R (eds) (2008) Mammals of Australia, 3rd edn. Reed New Holland, Sydney

    Google Scholar 

  • Vestjens WJM, Hall LS (1977) Stomach contents of forty-two species of bats from the Australasian region. Aust Wildl Res 4:25–35

    Article  Google Scholar 

  • Waters DA, Jones G (1995) Echolocation call structure and intensity in five species of insectivorous bats. J Exp Biol 198:475–489

    PubMed  CAS  Google Scholar 

  • Wilson DE (1973) Bat faunas: a trophic comparison. Syst Zool 22:14–29

    Article  Google Scholar 

  • Wyttenbach RA, May ML, Hoy RR (1996) Categorical perception of sound frequency by crickets. Science 273:1542–1544

    Article  PubMed  CAS  Google Scholar 

  • Zufall F, Schmitt M, Menzel R (1989) Spectral and polarized light sensitivity of photoreceptors in the compound eye of the cricket (Gryllus bimaculatus). J Comp Physiol A 164:597–608

    Article  PubMed  CAS  Google Scholar 

  • Zuk M, Rotenberry JT, Simmons LW (1998) Calling songs of field crickets (Teleogryllus oceanicus) with and without phonotactic parasitoid infection. Evolution 52:166–171

    Article  Google Scholar 

  • Zuk M, Rotenberry JT, Tinghitella RM (2006) Silent night: adaptive disappearance of a sexual signal in a parasitized population of field crickets. Biol Lett 2:521–524

    Article  PubMed  Google Scholar 

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Acknowledgments

Thanks to Reese Arh for data analysis and Peter Wall for the custom MATLAB sound-generating and spike analysis applications. The manuscript was greatly improved by comments from Holger Görlitz, Fernando Montealegre-Zappata, and two anonymous reviewers. Funding was provided by a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery grant to JHF, University of Toronto undergraduate research support to JK, and an NSERC postgraduate scholarship to HMtH.

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Correspondence to Hannah M. ter Hofstede.

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ter Hofstede, H.M., Killow, J. & Fullard, J.H. Gleaning bat echolocation calls do not elicit antipredator behaviour in the Pacific field cricket, Teleogryllus oceanicus (Orthoptera: Gryllidae). J Comp Physiol A 195, 769–776 (2009). https://doi.org/10.1007/s00359-009-0454-3

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