Advertisement

Journal of comparative physiology

, Volume 99, Issue 1, pp 1–66 | Cite as

Visual control of flight behaviour in the hoverflySyritta pipiens L.

  • T. S. Collett
  • M. F. Land
Article

Summary

  1. 1.

    The visually guided flight behaviour of groups of male and femaleSyritta pipiens was filmed at 50 f.p.s. and analysed frame by frame. Sometimes the flies cruise around ignoring each other. At other times males but not females track other flies closely, during which the body axis points accurately towards the leading fly.

     
  2. 2.

    The eyes of males but not females have a forward directed region of enlarged facets where the resolution is 2 to 3 times greater than elsewhere. The inter-ommatidial angle in this “fovea” is 0.6°.

     
  3. 3.

    Targets outside the fovea are fixated by accurately directed, intermittent, open-loop body saccades. Fixation of moving targets within the fovea is maintained by “continuous” tracking in which the angular position of the target on the retina (Θe) is continuously translated into the angular velocity of the tracking fly (\(\dot \Phi _p \)) with a latency of roughly 20 ms (\(\dot \Phi _p = k \Theta _e \), wherek≏30 s−1).

     
  4. 4.

    The tracking fly maintains a roughly constant distance (in the range 5–15 cm) from the target. If the distance between the two flies is more than some set value the fly moves forwards, if it is less the fly moves backwards. The forward or backward velocity (\(\dot F_p \)) increases with the difference (D-D0) between the actual and desired distance (\(\dot F_p = k^\prime (D - D_0 )\)), wherek′=10 to 20 s−1). It is argued that the fly computes distance by measuring the vertical substense of the target image on the retina.

     
  5. 5.

    Angular tracking is sometimes, at the tracking fly's choice,supplemented by changes in sideways velocity. The fly predicts a suitable sideways velocity probably on the basis of a running averageΘ e , but not its instantaneous value. Alternatively, when the target is almost stationary, angular tracking may bereplaced by sideways tracking. In this case the sideways velocity (\(\dot S\)) is related toΘ e about 30 ms earlier (\(\dot S_p = k\prime \prime \Theta _e \), wherek″=2.5 cm · s−1 · deg−1), and the angular tracking system is inoperative.

     
  6. 6.

    When the leading fly settles the tracking fly often moves rapidly sideways in an arc centred on the leading fly. During thesevoluntary sideways movements the male continues to point his head at the target. He does this not by correctingΘ e , which is usually zero, but by predicting the angular velocity needed to maintain fixation. This prediction requires knowledge of both the distance between the flies and the tracking fly's sideways velocity. It is shown that the fly tends to over-estimate distance by about 20%.

     
  7. 7.

    When two males meet head on during tracking the pursuit may be cut short as a result of vigorous sideways oscillations of both flies. These side-to-side movements are synchronised so that the males move in opposite directions, and the oscillations usually grow in size until the males separate. The angular tracking system is active during “wobbling” and it is shown that to synchronise the two flies the sideways tracking system must also be operative. The combined action of both systems in the two flies leads to instability and so provides a simple way of automatically separating two males.

     
  8. 8.

    Tracking is probably sexual in function and often culminates in a rapid dart towards the leading fly, after the latter has settled. During these “rapes” the male accelerates continuously at about 500 cm · s−2, turning just before it lands so that it is in the copulatory position. The male rapes flies of either sex indicating that successful copulation involves more trial and error than recognition.

     
  9. 9.

    During cruising flight the angular velocity of the fly is zero except for brief saccadic turns. There is often a sideways component to flight which means that the body axis is not necessarily in the direction of flight. Changes in flight direction are made either by means of saccades or by adjusting the ratio of sideways to forward velocity (\(\dot S/\dot F\)). Changes in body axis are frequently made without any change in the direction of flight. On these occasions, when the fly makes an angular saccade, it simultaneously adjusts\(\dot S/\dot F\) by an appropriate amount.

     
  10. 10.

    Flies change course when they approach flowers using the same variety of mechanisms: a series of saccades, adjustments to\(\dot S/\dot F\), or by a mixture of the two.

     
  11. 11.

    The optomotor response, which tends to prevent rotation except during saccades, is active both during cruising and tracking flight.

     

Keywords

Retina Angular Velocity Body Axis Flight Direction Forward Velocity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Barlow, H. B.: The size of ommatidia in apposition eyes. J. exp. Biol.59, 667–674 (1952)Google Scholar
  2. Barrós-Pita, J. C., Maldonado, H.: A fovea in the praying mantis eye. II. Some morphological characteristics. Z. vergl. Physiol.67, 79–92 (1970)Google Scholar
  3. Braitenberg, V., Hauser-Holschuh, H.: Patterns of projection in the visual system of the fly. II. Quantitative aspects of second order neurons in relation to models of movement perception. Exp. Brain Res.16, 184–209 (1972)PubMedGoogle Scholar
  4. Burkhardt, D., de la Motte, I., Seitz, G.: Physiological optics of the compound eye of the blow fly. In: The functional organization of the compound eye (ed. Bernhard, C. G.), p. 51–62. London: Pergamon Press 1966Google Scholar
  5. Camhi, J. M.: Neural mechanisms of response modification in insects. In: Experimental analysis of insect behaviour (ed. Barton Browne, L.), p. 60–86. Berlin-Heidelberg-New York: Springer 1974Google Scholar
  6. Collett, T. S., King, A. J.: Vision during flight. In: The compound eye (ed. G. A. Horridge). Oxford: University Press 1975Google Scholar
  7. Coggeshall, J. C.: The landing response and visual processing in the milkweed bug,Oncopeltus fasciatus. J. exp. Biol.57, 401–413 (1972)Google Scholar
  8. Dietrich, W.: Die Facettenaugen der Dipteren. Z. wiss. Zool.92, 465–539 (1909)Google Scholar
  9. Duelli, P.: The relation of astromenotactic and anemomenotactic orientation mechanisms in desert ants, Cataglyphisbicolor (Formicidae, Hymenoptera). In: Information processing in the visual systems of arthropods (ed. Wehner, R.), p. 281–286. Berlin-Heidelberg-New York: Springer 1972Google Scholar
  10. Easter, S. S., Johns, P. R., Heckenlively, D.: Horizontal compensatory eye movements in goldfish (Carassius auratus). I. The normal animal. J. comp. Physiol.92, 23–35 (1974)Google Scholar
  11. Franceschini, N., Kirschfeld, K.: Les phénomènes de pseudopupille dans l'oeil composé deDrosophila. Kybernetik9, 159–182 (1971)PubMedGoogle Scholar
  12. Frantsevich, L. I., Zolotov, V. V.: Turning dynamics in the phototaxis ofEristalis tenax L. (Diptera, Syrphidae). J. gen. Biol. Akad. Nauk. U.S.S.R.34, 654–660 [in Russian] (1973)Google Scholar
  13. Fuchs, A. F.: The saccadic system. In: The control of eye movements (eds. Bach-y-Rita, P., Collins, C.C., Hyde, J. E.), p. 343–362. New York: Academic Press 1971Google Scholar
  14. Gaffron, M.: Untersuchungen über das Bewegungssehen bei Libellenlarven, Fliegen und Fischen. Z. vergl. Physiol.20, 299–337 (1934)Google Scholar
  15. Goodman, L. J.: The landing responses of insects. I. The landing response of the flyLucilia sericata and other Calliphorinae. J. exp. Biol.37, 854–878 (1960)Google Scholar
  16. Hassenstein, B.: Information and control in the living organism. London: Chapman & Hall 1971Google Scholar
  17. Hoyle, G.: Exploration of neuronal mechanisms underlying behavior in insects. In: Neural theory and modelling (ed. Reiss, R. F., p. 346–376. Stanford: Stanford University Press 1964Google Scholar
  18. Land, M. F.: Stepping movements made by jumping spiders during turns mediated by the lateral eyes. J. exp. Biol.57, 15–40 (1972)PubMedGoogle Scholar
  19. Land, M. F.: Head movement of flies during visually guided flight. Nature (Lond.)243, 299–300 (1973)Google Scholar
  20. Land, M. F., Collett, T. S.: Chasing behaviour of houseflies (Fannia canicularis). A description and analysis. J. comp. Physiol.89, 331–357 (1974)Google Scholar
  21. Lindauer, M.: Behavior of bees under optical learning conditions. In: Processing of optical data by organisms and machines (ed. Reichardt, W.), p. 527–543. New York: Academic Press 1969Google Scholar
  22. Maldonado, H., Barrós-Pita, J. C.: A fovea in the praying mantis eye. I. Estimation of the catching distance. Z. vergl. Physiol.67, 58–78 (1970)Google Scholar
  23. Mittelstaedt, H.: Prey capture in mantids. In: Recent advances in invertebrate physiology (ed. Scheer, B. T.), p. 51–71. Eugene: University of Oregon Press 1957Google Scholar
  24. Mittelstaedt, H.: Basic control patterns of orientational homeostasis. Symp. Soc. exp. Biol.18, 365–385 (1964)PubMedGoogle Scholar
  25. Morasso, P., Bizzi, E., Dichgans, J.: Adjustment of saccade characteristics during head movements. Exp. Brain Res.16, 492–500 (1973)PubMedGoogle Scholar
  26. Parmenter, L.: Behaviour ofSyritta pipiens L. (Dipt., Syrphidae). Entom. Monthly Mag. (U.K.)80, 44 (1944)Google Scholar
  27. Poggio, T., Reichardt, W.: A theory of the pattern induced flight orientation of the flyMusca domestica. Kybernetik12, 185–203 (1973)PubMedGoogle Scholar
  28. Reichardt, W.: The insect eye as a model for analysis of uptake, transduction, and processing of optical data in the nervous system. In: The neurosciences, second study program (ed. Schmitt, F. O.), p. 494–511. New York: Rockefeller University Press 1970Google Scholar
  29. Reichardt, W., Wenking, H.: Optical detection and fixation of objects by fixed flying flies. Naturwissenschaften56, 424–425 (1969)Google Scholar
  30. Richards, O. W.: Sexual selection and allied problems in insects. Biol. Rev.2, 298–364 (1927)Google Scholar
  31. Robinson, D. A.: The oculomotor control system: a review. Proc. Inst. Elec. Electron. Eng.56, 1632–1639 (1968)Google Scholar
  32. Robinson, D. A.: Models of oculomotor neural organization. In: The control of eye movements (eds. Bach-y-Rita, P., Collins, C. C., Hyde, J. E.), p. 519–538. New York: Academic Press 1971Google Scholar
  33. Stark, L.: The control system for versional eye movements. In: The control of eye movements (eds. Bach-y-Rita, P., Collins, C. C., Hyde, J. E.), p. 363–428. New York: Academic Press 1971Google Scholar
  34. Steinbach, M. J.: Eye tracking of self-moved targets: the role of efference. J. exp. Psychol.82, 366–376 (1969)PubMedGoogle Scholar
  35. Strausfeld, N. J.: Golgi studies on insects. II. The optic lobes of Diptera. Phil. Trans. B258, 135–223 (1970)Google Scholar
  36. Strausfeld, N. J.: The organization of the insect visual system (light microscopy). I. Projections and arrangements of neurons in the lamina ganglionaris of Diptera. Z. Zellforsch.121, 377–441 (1971)Google Scholar
  37. Tansley, K.: Vision in vertebrates. London: Chapman & Hall 1965Google Scholar
  38. Virsik, R., Reichardt, W.: Tracking of moving objects by the flyMusca domestica. Naturwissenschaften61, 132–133 (1974)Google Scholar
  39. Vogel, G.: Verhaltensphysiologische Untersuchungen über die den Weibchenbesprung des Stubenfliegen-Männchens (Musca domestica) auslösenden optischen Faktoren. Z. Tierpsychol.14, 309–323 (1957)Google Scholar
  40. Walls, G. L.: The vertebrate eye. New York: Haffner Publishing Co. 1963Google Scholar
  41. Wehner, R., Flatt, I.: The visual orientation of desert ants,Cataglyphis bicolor, by means of terrestrial cues. In: Information processing in the visual systems of arthropods (ed. Wehner, R.), p. 295–302. Berlin-Heidelberg-New York: Springer 1972Google Scholar
  42. Weis-Fogh, T.: Quick estimates of flight fitness in hovering animals, including novel mechanisms for lift production. J. exp. Biol.59, 169–230 (1973)Google Scholar
  43. Westheimer, G., Conover, D. W.: Smooth eye movements in the absence of a moving visual stimulus. J. exp. Psychol.47, 283–284 (1954)PubMedGoogle Scholar
  44. Wickler, W., Seibt, U.: Zur Ethologie afrikanischer Stielaugenfliegen (Diptera, Diopsidae). Z. Tierpsychol.31, 113–130 (1972)Google Scholar
  45. Wilson, D. M.: Inherent asymmetry and reflex modulation of the locust flight motor pattern. J. exp. Biol.48, 631–641 (1968)PubMedGoogle Scholar
  46. Wilson, D. M., Hoy, R. R.: Optomotor reaction, locomotory bias and reactive inhibition in the milkweed bugOncopeltus and the beetleZophobas. Z. vergl. Physiol.58, 136–152 (1968)Google Scholar
  47. Yarbus, A. L.: Eye movements and vision. New York: Plenum Press 1967Google Scholar
  48. Young, L. R.: Pursuit eye tracking movements. In: The control of eye movements (ed. Bach-y-Rita, P., Collins, C. C., Hyde, J. E.), p. 429–443. New York: Academic Press 1971Google Scholar

Copyright information

© Springer-Verlag 1975

Authors and Affiliations

  • T. S. Collett
    • 1
  • M. F. Land
    • 1
  1. 1.School of Biological SciencesUniversity of SussexBrightonUK

Personalised recommendations