Skip to main content
Log in

Locust flight steering

I. Head movements and the organization of correctional manoeuvres

  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Summary

Locusts (Locusta migratoria) were flown in a flight simulator which converts yaw torque into angular motion of the visual environment (Fig. 1). The modalities and the time-course of steering behavior under these closed-loop conditions have been investigated.

  1. 1.

    Locusts flying under visual closed-loop conditions stabilize their visual environment by performing correctional steering manoeuvres. Besides torque production, due to differential wing movements and ruddering, correctional steering also involves head movements (Fig. 6).

  2. 2.

    During open-loop steering, ruddering and yaw torque begin some 60 ms after the onset of the visually simulated deviation from course. Head movements occur some 90 ms after stimulus onset, i.e. some 30 ms later than yaw torque (Figs. 3, 5) and therefore do not initiate thoracic steering outputs.

  3. 3.

    Open- and closed-loop correctional steering do not differ in their behavioral components or temporal organization (Figs. 2, 6, Table 1).

  4. 4.

    In the absence of major disturbances, correctional steering under closed-loop conditions is performed with minimal ruddering (only a few degrees in amplitude), that probably produces little or no aerodynamic drag (Fig. 6).

  5. 5.

    Locusts prevented from moving their heads still stabilize their visual environment in the closed-loop situation. However, the precision of steering is affected by this constraint (Figs. 8, 9, 10, 12). Head immobilization also alters the temporal coordination of correctional steering (Figs. 7, 11).

  6. 6.

    These results show that head movements, in addition to their generally accepted role in vision improvement, also contribute to the precision and temporal coordination of correctional flight manoeuvres. The mechanism is partly via proprioceptive feedback.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Arbas EA (1986) Control of hindlimb posture by wind-sensitive hairs and antennae during locust flight. J Comp Physiol A 159:849–857

    Google Scholar 

  • Baader A (1991) Auditory interneurons in locusts produce directional head and abdomen movements. J Comp Physiol A 169:87–100

    Google Scholar 

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

    Google Scholar 

  • Boyan GS, Ashman S, Ball EE (1986) Initiation and modulation of flight by a single giant interneuron in the cercal system of the locust. Naturwissenschaften 73:272–274

    Google Scholar 

  • Camhi JM (1970a) Yaw-correcting postural changes in locusts. J Exp Biol 52: 519–531

    Google Scholar 

  • Camhi JM (1970b) Sensory control of abdomen posture in flying locusts. J Exp Biol 52:533–537

    Google Scholar 

  • Collett TS (1980) Angular tracking and the optomotor response. An analysis of visual reflex interaction in a hoverfly. J Comp Physiol 140:145–158

    Google Scholar 

  • Dugard JJ (1967) Directional change in flying locusts. J Insect Physiol 13:1055–1063

    Google Scholar 

  • Forman R, Brumbley D (1980) An improved capacitive position transducer for biological systems. J Exp Biol 88: 399–402

    Google Scholar 

  • Fraser PJ (1977) Cercal ablation modifies tethered flight behaviour of cockroach. Nature 268:523

    Google Scholar 

  • Geiger G, Poggio T (1977) On head and body movements of flying flies. Biol Cybern 25:177–180

    Google Scholar 

  • Gewecke M, Philippen J (1978) Control of the horizontal flight course by air-current sense organs in Locusta migratoria. Physiol Entomol 3:43–52

    Google Scholar 

  • Goodman LJ (1959) Hair receptors in locusts. Hair plates on the first cervical sclerites of the Orthoptera. Nature 183:1106–1107

    Google Scholar 

  • Goodman LJ (1965) The role of certain optomotor reactions in regulating stability in the rolling plane during flight in the desert locust, Schistocerca gregaria. J Exp Biol 42:385–407

    Google Scholar 

  • Götz KG (1987) Course-control metabolism and wing interference during ultralong tethered flight in Drosophila melanogaster. J Exp Biol 128: 35–46

    Google Scholar 

  • Hengstenberg R (1988) Mechanosensory control of compensatory head roll during flight in the blowfly Calliphora erythrocephala Meig. J Comp Physiol A 163:151–165

    Google Scholar 

  • Hensler K (1988) The pars intercerebralis neurone PI(2)5 of locusts: convergent processing of inputs reporting head movements and deviations from straight flight. J Exp Biol 140:511–533

    Google Scholar 

  • Hensler K (1989) Corrective flight steering in locusts: convergence of extero- and proprioceptive inputs in descending deviation detectors. In: Naresh Singh R, Strausfeld NJ (eds) Neurobiology of sensory systems. Plenum, New York, pp 531–554

    Google Scholar 

  • Hensler K, Robert D (1990) Compensatory head rolling during corrective flight steering in locusts. J Comp Physiol A 166:685–693

    Google Scholar 

  • Land MF (1975) Head movements and fly vision. In: Horridge A (ed) The compound eye and vision of insects. Clarendon Press, Oxford, pp 469–489

    Google Scholar 

  • Miall RC (1989) A systems analysis of the role of head position during steering in locust flight. In: Erber J, Menzel R, Pflüger H-J, Todt D (eds) Neural mechanisms of behavior. Proc. 2nd Internat Congr Neuroethology. Thieme, Stuttgart New York, Abstract 2

    Google Scholar 

  • Miall RC (1990) Visual control of steering in locusts: the effects of head movement on responses to roll stimuli. J Comp Physiol A 166:735–744

    Google Scholar 

  • Mittelstaedt H (1950) Physiologie des Gleichgewichtssinnes bei fliegenden Libellen. Z Vergl Physiol 32:422–463

    Google Scholar 

  • Möhl B (1988) Short term learning during flight control in Locusta migratoria. J Comp Physiol A 163:803–812

    Google Scholar 

  • Reichardt W (1973) Musterinduzierte Flugorientierung der Fliege Musca domestica. Naturwissenschaften 60:122

    Google Scholar 

  • Reichardt W, Wenking H (1969) Optical detection and fixation of objects by fixed flying flies. Naturwissenschaften 56:424–425

    Google Scholar 

  • Reichert H, Rowell CHF (1985) Integration of non-phaselocked exteroceptive information in the control of rhythmic flight in the locust. Neurophysiol 5:1201–1218

    Google Scholar 

  • Reichert H, Rowell CHF, Griss C (1985) Course-correction circuitry translates feature detection into behavioural action in locusts. Nature 315:142–144

    Google Scholar 

  • Robert D (1988) Visual steering under closed-loop conditions by flying locusts: flexibility of optomotor response and mechanisms of correctional steering. J Comp Physiol A 164:15–24

    Google Scholar 

  • Rowell CHF (1988) Mechanisms of flight steering in locusts. Experientia 44:389–395

    Google Scholar 

  • Rowell CHF (1989) Descending interneurones reporting deviation from flight course: what is their role in steering? J Exp Biol 146:177–194

    Google Scholar 

  • Rowell CHF, Pearson KG (1983) Ocellar input to the flight motor system of the locust: structure and function. J Exp Biol 103:265–288

    Google Scholar 

  • Rowell CHF, Reichert H (1986) Three descending interneurons reporting deviation from course in the locust. II. Physiology. J Comp Physiol A 158:775–794

    Google Scholar 

  • Schmidt J, Zarnack W (1987) The motor pattern of locusts during visually induced rolling in long-term flight. Biol Cybern 56:397–410

    Google Scholar 

  • Shepheard P (1973) Musculature and innervation of the neck of the locust, Schistocerca gregaria (Forskål). J Morphology 139:439–464

    Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry. Second edition. WH Freeman and Company, New York

    Google Scholar 

  • Sotavalta O (1947) The flight-tone (wingbeat frequency) of insects. Acta Entomol Fennica 4:1–115

    Google Scholar 

  • Taylor CP (1981a) Contribution of compound eyes and ocelli to steering of locusts in flight. I. Behavioural analysis. J Exp Biol 93:1–18

    Google Scholar 

  • Taylor CP (1981b) Contribution of compound eyes and ocelli to steering of locusts in flight. II. Timing changes in flight motor units. J Exp Biol 93:19–31

    Google Scholar 

  • Thüring DA (1986) Variability of the motor output during flight steering in locusts. J Comp Physiol A 156:655–664

    Google Scholar 

  • Tomioka K, Yamaguchi T (1980) Steering responses of adult and nymphal crickets to light, with special reference to the head rolling movement. J Insect Physiol 26:47–57

    Google Scholar 

  • Wilson DM (1968) Inherent asymmetry and reflex modulation of the locust flight motor pattern. J Exp Biol 48:631–641

    Google Scholar 

  • Zarnack W, Möhl B (1977) Activity of the direct downstroke flight muscles of Locusta migratoria (L.) during steering behaviour in flight. I: Patterns of time shift. J Comp Physiol 118:215–233

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Robert, D., Rowell, C.H.F. Locust flight steering. J Comp Physiol A 171, 41–51 (1992). https://doi.org/10.1007/BF00195959

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00195959

Key words

Navigation