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Gliding behaviour elicited by lateral looming stimuli in flying locusts

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Abstract

We challenged tethered, flying locusts with visual stimuli looming from the side towards one eye in a way that mimics the approach of a predatory bird. Locusts respond to the lateral approach of a looming object with steering movements and a stereotyped, rapid behaviour in which the wingbeat pattern ceases and the wings are swept into a gliding posture. This gliding behaviour may cause the locust to dive. The gliding posture is maintained for 200 ms or more after which flight is resumed with an increased wingbeat frequency or else the wings are folded. A glide begins with a strong burst of activity in the mesothoracic second tergosternal motor neuron (no. 84) on both sides of the locust. Recordings of descending contralateral movement detector (DCMD) activity in a flying locust show that it responds to small (80-mm diameter) looming stimuli during tethered flight, with a prolonged burst of spikes that tracks stimulus approach and reaches peak instantaneous frequencies as, or after, stimulus motion ceases. There is a close match between the visual stimuli that elicit a gliding behaviour and those that are effective at exciting the DCMD neuron. Wing elevation into the gliding posture occurs during a maintained burst of high frequency DCMD spikes.

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Abbreviations

DCMD:

Descending contralateral movement detector

EMG:

Electromyogram

IR:

Infra-red

LGMD:

Lobula giant movement detector

MN:

Motor neuron

References

  • Baker PS, Cooter RJ (1979a) The natural flight of the migratory locust, Locusta migratoria L. I. Wing movements. J Comp Physiol A 131:79–87

    Google Scholar 

  • Baker PS, Cooter RJ (1979b) The natural flight of the migratory locust, Locusta migratoria L. II. Gliding. J Comp Physiol A 131:89–94

    Google Scholar 

  • Baker PS, Gewecke M, Cooter RJ (1981) The natural flight of the migratory locust, Locusta migratoria L. III. Wing-beat frequency, flight speed and attitude. J Comp Physiol A 141:233–237

    Google Scholar 

  • Boyan GS (1989) Synaptic input converging onto an identified premotor interneuron in the locust is gated according to modality. Naturwissenschaften 76:431–433

    Article  Google Scholar 

  • Burrows M, Rowell CHF (1973) Connections between descending visual interneurons and metathoracic motoneurons in the locust. J Comp Physiol A 85:221–234

    Google Scholar 

  • Camhi JM, Tom W, Volman S (1978) The escape behaviour of the cockroach Periplaneta americana II. Detection of natural predators by air displacement. J Comp Physiol A 128:203–212

    Google Scholar 

  • Casas J (2004) Air flow sensing: from physical ecology in the field to nanotech implementation. Presented at the 7th congress of the International Society for Neuroethology, Denmark. Neuromorphic Approaches to Neuroethology Abstract SY38

    Google Scholar 

  • Cloupeau M, Devillers JF, Devezeaux D (1979) Direct measurements of instantaneous lift in desert locust; comparison with Jensen’s experiments on detached wings. J Exp Biol 80:1–15

    Google Scholar 

  • Cramp S (1977) Handbook of the Birds of Europe, the Middle East and North Africa. The birds of the Western Paleartic. Oxford University Press, New York

    Google Scholar 

  • Dawson JW, Kutsch W, Robertson RM (2004) Auditory-evoked evasive manoeuvres in free-flying locusts and moths. J Comp Physiol A 190:69–84

    Article  CAS  Google Scholar 

  • Fry CH, Fry K (1992) Kingfishers, bee-eaters and rollers. Christopher Helm A&C Black, London

    Google Scholar 

  • Gabbiani F, Krapp HG, Laurent G (1999) Computation of object approach by a wide-field motion-sensitive neuron. J Neurosci 19:1122–1141

    CAS  PubMed  Google Scholar 

  • Gibson JJ (1958) Visually controlled locomotion and visual orientation in animals. Br J Psychol 49:182–194

    CAS  PubMed  Google Scholar 

  • Gray JR, Lee JK, Robertson RM (2001) Activity of descending contralateral movement detector neurons and collision avoidance behaviour in response to head-on visual stimuli in locusts. J Comp Physiol A 187:115–129

    Article  Google Scholar 

  • Herberholz J, Sen MM, Edwards DH (2004) Behavioural and neural responses in crayfish to attacks from a natural predator. Presented at the 7th Congress of the International Society for Neuroethology, Denmark. Muscle, Motor and Sensory-Motor Systems Abstract PO233

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

    CAS  PubMed  Google Scholar 

  • Hudleston JA (1958) Some notes on the effects of bird predators on hopper bands of the desert locust (Schistocerca gregaria Forskal). Entomol Monthly Mag 94:210–214

    Google Scholar 

  • Jensen M (1956) Biology and physics of locust flight III. The aerodynamics of locust flight. Philos Trans R Soc Lond B 239:511–552

    Google Scholar 

  • Judge SJ, Rind FC (1997) The locust DCMD, a movement-detecting neurone tightly tuned to collision trajectories. J Exp Biol 200:2209–2216

    PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Miller LA (1975) The behaviour of flying green lacewings, Chrysopa carnea, in the presence of ultrasound. J Insect Physiol 21:205–219

    Article  Google Scholar 

  • Nickerson B (1958) Some observations of the carmine bee-eater Merops nubicus Gmelin in the French Sudan. Ibis 100:454–457

    Google Scholar 

  • O’Shea M, Rowell CHF (1975) A spike-transmitting electrical synapse between visual interneurons in the locust movement detector system. J Comp Physiol A 97:143–158

    Google Scholar 

  • O’Shea M, Rowell CHF, Williams JLD (1974) The anatomy of a locust visual interneurone: the descending contralateral movement detector. J Exp Biol 60:1–12

    Google Scholar 

  • Pearson KG, Boyan GS, Bastiani M, Goodman CS (1985) Heterogenous properties of segmentally homologous interneurons in the ventral nerve cord of locusts. J Comp Neurol 233:133–145

    CAS  PubMed  Google Scholar 

  • Pfau HK (1977) Zur Morphologie und Funktion des Vorderfügels und Vorderfügelgelenks von Locusta migratoria L. Fortschr Zool 24:341–345

    Google Scholar 

  • Pond CM (1972) Neuromuscular activity and wing movements at the start of flight of Periplaneta americana and Schistocerca gregaria. J Comp Physiol 78:192–209

    Google Scholar 

  • Reichert H, Rowell CHF (1985) Integration of nonphaselocked exteroceptive information in the control of rhythmic flight in the locust. J Neurophysiol 53:1201–1218

    Google Scholar 

  • Reichert H, Rowell CHF (1986) Neuronal circuits controlling flight in the locust: how sensory information is processed for motor control. Trends Neurosci 9:281–283

    Article  Google Scholar 

  • Rind FC (1984) A chemical synapse between two motion detecting neurons in the locust brain. J Exp Biol 110:143–167

    CAS  PubMed  Google Scholar 

  • Rind FC, Santer RD (2004) Collision avoidance and a looming sensitive neuron: size matters but biggest is not necessarily best. Proc R Soc Lond B 271:S27-S29

    Article  PubMed  Google Scholar 

  • Rind FC, Simmons PJ (1992) Orthopteran DCMD neuron: a reevaluation of responses to moving objects. I. Selective responses to approaching objects. J Neurophysiol 68:1654–1666

    Google Scholar 

  • Robert D (1989) The auditory behaviour of flying locusts. J Exp Biol 147:279–301

    Google Scholar 

  • Robertson RM, Johnson AG (1993) Collision avoidance of flying locusts: steering torques and behaviour. J Exp Biol 183:35–60

    Google Scholar 

  • Robertson RM, Reye DN (1992) Wing movements associated with collision-avoidance manoeuvres during flight in the locust Locusta migratoria. J Exp Biol 163:231–258

    Google Scholar 

  • Roeder KD (1962) The behaviour of free flying moths in the presence of artificial ultrasonic pulses. Anim Behav 10:300–304

    Google Scholar 

  • Roeder KD (1967) Nerve cells and insect behaviour. Harvard University Press, Cambridge

    Google Scholar 

  • Schlotterer GR (1977) Response of the locust descending movement detector neuron to rapidly approaching and withdrawing visual stimuli. Can J Zool 55:1372–1376

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Simmons PJ (1980a) A locust wind and ocellar brain neurone. J Exp Biol 85:281–294

    Google Scholar 

  • Simmons PJ (1980b) Connexions between a movement-detecting visual interneurone and flight motoneurones of a locust. J Exp Biol 86:87–97

    Google Scholar 

  • Simmons PJ, Rind FC (1992) Orthopteran DCMD neuron: a reevaluation of responses to moving objects. II. Critical cues for detecting approaching objects. J Neurophysiol 68:1667–1682

    Google Scholar 

  • Simmons PJ, Rind FC (1997) Responses to object approach by a wide field visual neurone, the LGMD2 of the locust: characterization and image cues. J Comp Physiol A 180:203–214

    Article  Google Scholar 

  • Smith KD, Popov GB (1953) On birds attacking desert locust swarms in Eritrea. The Entomologist 86:3–7

    Google Scholar 

  • Snodgrass RE (1929) The thoracic mechanism of a grasshopper and its antecedents. Smithson. Misc Collns 82:1–111

    Google Scholar 

  • Symmons PM, Cressman K (2001) Desert locust guidelines 1. Biology and behaviour. Food and Agriculture Organisation of the United Nations, Rome

    Google Scholar 

  • Thomas ALR, Taylor GK (2001) Animal flight dynamics I. Stability in gliding flight. J Theor Biol 212:399–424

    Article  CAS  PubMed  Google Scholar 

  • Weis-Fogh T (1956) Biology and physics of locust flight II. Flight performance of the desert locust (Schistocerca Gregaria). Philos Trans R Soc Lond B 239:459–510

    Google Scholar 

  • Wheatstone C (1852) Contributions to the physiology of vision. II. Philos Trans R Soc Lond B 142:1–18

    Google Scholar 

  • Yager DD, May ML (1990) Ultrasound-triggered, flight-gated evasive maneuvers in the praying mantis Parasphendale agrionina II. Tethered flight. J Exp Biol 152:41–58

    CAS  PubMed  Google Scholar 

  • Yager DD, May ML, Fenton MB (1990) Ultrasound-triggered, flight-gated evasive maneuvers in the praying mantis Parasphendale agrionina I. Free flight. J Exp Biol 152:17–39

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Supported by the Gatsby Charitable Foundation and the BBSRC (Grant 13/S17899). We thank Dr. Jeremy Thomason for the use of the high-speed camera equipment in preliminary experiments, Bob McGowan (National Museums of Scotland) and John Curton (Columbus Zoo and Aquarium) for providing the carmine bee-eater measurements, and Dr. Hanno Fischer for helpful discussions. The experiments described in this manuscript comply with the ‘Principles of animal care’, publication No. 86-23 revised 1985, of the National Institute of Health and also with the current laws of the UK.

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  1. School of Biology, University of Newcastle, Ridley Building, Newcastle upon tyne, NE1 7RU, UK

    Roger D. Santer, Peter J. Simmons & F. Claire Rind

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  1. Roger D. Santer
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  2. Peter J. Simmons
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  3. F. Claire Rind
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Correspondence to Roger D. Santer.

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Santer, R.D., Simmons, P.J. & Rind, F.C. Gliding behaviour elicited by lateral looming stimuli in flying locusts. J Comp Physiol A 191, 61–73 (2005). https://doi.org/10.1007/s00359-004-0572-x

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  • DOI: https://doi.org/10.1007/s00359-004-0572-x

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