Journal of Comparative Physiology A

, Volume 163, Issue 2, pp 151–165 | Cite as

Mechanosensory control of compensatory head roll during flight in the blowflyCalliphora erythrocephala Meig.

  • Roland Hengstenberg


  1. 1.

    In the blowflyCalliphora flying stationarily in a wind tunnel, compensatory head movements were elicited by rolling the fly about its longitudinal axis (Fig. 1). Responses were recorded on video tape, and evaluated by single frame analysis.

  2. 2.

    Active head movements were observed in response to visual and mechanosensory stimuli (Fig. 2). They are not made or caused by the head's inertial momentum (Fig. 11).

  3. 3.

    Gravity, used by walking flies to align their head with the vertical, does not seem to be perceived during flight (Figs. 3–6) but has a passive stabilizing effect upon the flight attitude (Fig. 7).

  4. 4.

    A difference in aerodynamical load of the two wings elicits a transient head roll partly compensating a banked attitude (Figs. 4–6). The majority of campaniform sensilla at the wing base seems suitable to measure wing load.

  5. 5.

    Steady roll motion elicits a steady compensatory head roll which does not vanish even after 8 min of rotation at constant angular velocity (Fig. 8). Roll motion is most efficient at high roll speeds (100‡/s<w<2000‡/s). Mechanical motion perception fails if both halteres are disabled by arresting their oscillation or by amputation of the haltere knobs (Fig. 11). Flies with only one haltere intact cannot distinguish pitch from roll, but with respect to the sense of rotation they still respond bidirectionally (Fig. 12). Haltere dynamics and the response characteristics of haltere sensilla are discussed on the basis of recent results.

  6. 6.

    Head/body coordination is demonstrated in the absence of any roll stimulus (Fig. 3 a). The role of resilience of the neck skeleton, and that of different neck sense organs are discussed.

  7. 7.

    Mechanosensory roll control inCalliphora depends upon the locomotor state: When walking, the fly aligns its head vertically by gravity perception (Horn 1982). When flying, it controls only fast rotations. Passive attitude stabilization and visual means of control are required to maintain an upright flight attitude and head orientation.



Roll Motion Aerodynamical Load Wing Load Wing Base Head Roll 



number of flies/experiment


number of measurements or incidence


standard deviation of measurement


standard error of the mean

HP, TP, PP (‡)

roll angle of the fly's head, its thorax, and of the pattern relative to the vertical. Upwards is zero

HV, TV, PV (‡/s)

are the corresponding angular velocities. The sign of rotations is positive for rolls to the right i.e. clockwise when looking in flight direction


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  1. Barth FG (1986) Zur Organisation sensorischer Systeme: die cuticulären Mechanorezeptoren der Arthropoden. Verh Dtsch Zool Ges 79:69–90Google Scholar
  2. Buddenbrock W von (1919) Die vermutliche Lösung der Halterenfrage. Pflügers Arch 175:125–164Google Scholar
  3. Carpenter RHS (1977) Movements of the eyes. Pion, LondonGoogle Scholar
  4. Collett T (1987) Binocular depth vision in arthropods. TINS 10:1–2Google Scholar
  5. Collewijn H (1970) Oculomotor reactions in the cuttlefishSepia officinalis. J Exp Biol 52:369–384Google Scholar
  6. Dieringer N (1986) Vergleichende Neurobiologie von blickstabilisierenden Reflexsystemen bei Wirbeltieren. Naturwissenschaften 73:299–304Google Scholar
  7. Faust R (1952) Untersuchungen zum Halterenproblem. Zool Jahrb Physiol 63:325–366Google Scholar
  8. Fraenkel G (1932) Untersuchungen über die Koordination von Reflexen und automatisch-nervösen Rhythmen bei Insekten. 1. Die Flugreflexe der Insekten und ihre Koordination. Z Vergl Physiol 16:371–393Google Scholar
  9. Fudalewicz-Niemczyk W (1963) L'innervation et les organes sensoriels des ailes des Diptères et comparaison avec l'innervation des ailes d'autres ordres. Acta Zool Cracov 8:351–462Google Scholar
  10. Geiger G, Poggio T (1977) On head and body movements of flying flies. Biol Cybern 25:177–180Google Scholar
  11. Gettrup E (1966) Sensory regulation of wing twisting in locusts. J Exp Biol 44:1–16Google Scholar
  12. Gewecke M (1967) Die Wirkung von Luftströmung auf die Antennen und das Flugverhalten der blauen Schmeißfliege (Calliphora erythrocephala). Z Vergl Physiol 54:121–164Google Scholar
  13. Gnatzy W, Grünert U, Bender M (1987) Campaniform sensilla ofCalliphora vicina (Insecta, Diptera). I. Topography. Zoomorphology 106:312–319Google Scholar
  14. Goodman LJ (1965) The role of certain optomotor reactions in regulating stability in the rolling plane during flight in the desert locustSchistocerca gregaria. J Exp Biol 42:385–407Google Scholar
  15. Hain TC (1986) A model of the nystagmus induced by off vertical axis rotation. Biol Cybern 54:337–350Google Scholar
  16. Heide G (1974) The influence of wingbeat-synchronous feedback on the motor output systems in flies. Z Naturforsch 29c:739–744Google Scholar
  17. Heide G (1983) Neural mechanisms of flight control in Diptera. In: Nachtigall W (ed) Insect flight. Fischer, Stuttgart New York (BIONA report 2, pp 35–52)Google Scholar
  18. Hengstenberg R (1983) Zeitstrukturen der spontanen Flugaktivität vonCalliphora. Verh Dtsch Zool Ges 76:246Google Scholar
  19. Hengstenberg R (1984) Roll-stabilization during flight of the blowfly's head and body by mechanical and visual cues. In: VarjÚ D, Schnitzler H (eds) Localization and orientation in biology and engineering. Springer, Berlin Heidelberg New York, pp 121–134Google Scholar
  20. Hengstenberg R, Sandeman DC (1982) Kompensatorische Kopf-Roll-Bewegungen von Fliegen. Verh Dtsch Zool Ges 75:313Google Scholar
  21. Hengstenberg R, Sandeman DC, Hengstenberg B (1986) Compensatory head roll in the blowflyCalliphora during flight. Proc R Soc Lond B 227:455–482Google Scholar
  22. Hirth C (1981) Elektrophysiologische Untersuchungen über die Bildung der Impulsmuster in den neuromotorischen Systemen nicht-fibrillärer Flugmuskeln von Schmeißfliegen (Calliphora). Dissertation, Universität DüsseldorfGoogle Scholar
  23. Horn E (1975) The contribution of different receptors in gravity orientation in insects. Fortschr Zool 23:1–20Google Scholar
  24. Horn E (1982) Gravity reception in the walking flyCalliphora erythrocephala: tonic and modulatory influence of leg afferents on the head position. J Insect Physiol 28:713–721Google Scholar
  25. Horn E, Bischof HJ (1983) Gravity reception in crickets: The influene of cereal and antennal afferences on the head position. J Comp Physiol 150:93–98Google Scholar
  26. Horn E, Knapp A (1984) On the invariance of visual stimulus efficacy with respect to variable spatial positions. Behavioural investigations with flies (Calliphora erythrocephala). J Comp Physiol A 154:555–567Google Scholar
  27. Horn E, Lang H (1978) Positional head reflexes and the role of the prosternal organ in the walking flyCalliphora erythrocephala. J Comp Physiol 126:137–146Google Scholar
  28. Horsmann U, Wendler G (1985) The role of a fast wing reflex in locust flight. In: Gewecke M, Wendler G (eds) Insect locomotion. Paul Parey, Berlin, pp 157–165Google Scholar
  29. Ishay JS, Shimony BT, Arcan L (1983) The presence of statocysts and statoliths in social wasps (Hymenoptera, Vespinae). Life Sci 32:1711–1719Google Scholar
  30. Jander R, Schweder M (1971) über das Formunterscheidungsvermögen der SchmeißfliegeCalliphora erythrocephala. Z Vergl Physiol 72:186–196Google Scholar
  31. Kirmse W, Lässig P (1971) Strukturanalogie zwischen dem System der horizontalen Blickbewegungen beim Menschen und dem System der Blickbewegungen des Kopfes bei Insekten mit Fixationsreaktionen. Biol Zbl 90:175–193Google Scholar
  32. Koenderink JJ (1986) Optic flow. Vision Res 25:161–180Google Scholar
  33. Land MF (1975) Head movements and fly vision. In: Horridge GA (ed) The compound eye and vision of insects. Clarendon Press, Oxford, pp 469–489Google Scholar
  34. Lindauer M, Nedel JO (1959) Ein Schweresinnesorgan der Honigbiene. Z Vergl Physiol 42:334–364Google Scholar
  35. Liske E (1977) The influence of head position on the flight behaviour of the flyCalliphora erythrocephala. J Insect Physiol 23:375–379Google Scholar
  36. Liske E (1978) Der Einfluß gerichteter Kopfbewegungen auf das Flugsteuerungssystem der SchmeißfliegeCalliphora erythrocephala — Steuerung des Fluges durch die Augen und durch mechanorezeptorische Sinnesorgane. Dissertation, Universität DarmstadtGoogle Scholar
  37. Longuet-Higgins HC, Prazdny K (1980) The interpretation of moving retinal images. Proc R Soc Lond B 208:385–397Google Scholar
  38. Markl H (1962) Borstenfelder an den Gelenken als Schweresinnesorgane bei Ameisen und anderen Hymenopteren. Z Vergl Physiol 45:475–569Google Scholar
  39. Markl H (1974) The perception of gravity and of angular acceleration in invertebrates. In: Kornhuber HH (ed) Handbook of sensory physiology, vol VI/1. Springer, Berlin Heidelberg New York, pp 17–74Google Scholar
  40. Messenger JB (1981) Comparative physiology of vision in molluscs. In: Autrum H (ed) Handbook of sensory physiology, vol VII/6C. Springer, Berlin Heidelberg New York, pp 93–200Google Scholar
  41. Milde JJ, Seyan HS, Strausfeld NJ (1987) The neck motor system of the flyCalliphora erythrocephala. II. Sensory organization. J Comp Physiol A 160:225–238Google Scholar
  42. Mittelstaedt H (1950) Physiologie des Gleichgewichtssinnes bei fliegenden Libellen. Z Vergl Physiol 32:422–463Google Scholar
  43. Mittelstaedt H (1983) A new solution to the problem of the subjective vertical. Naturwissenschaften 70:272–281Google Scholar
  44. Nalbach G (1985) Die Haltere als Drehsinnesorgan. Wiss Arbeit, FB Biologie, Universität TübingenGoogle Scholar
  45. Nalbach G, Hengstenberg R (1986) Die Halteren vonCalliphora als Drehsinnesorgan. Verh Dtsch Zool Ges 79:229Google Scholar
  46. Neil DM, Schöne H, Scapini F, Miyan JA (1983) Optokinetic responses, visual adaptation, and multisensory control of eye movements in the spiny lobster,Palinurus vulgaris. J Exp Biol 107:349–366Google Scholar
  47. Nicklaus R (1968) Zur Funktion der keulenförmigen Sensillen auf den Cerci der Grillen. Verh Dtsch Zool Ges 393–398Google Scholar
  48. Peters W (1962) Die propriozeptiven Organe am Prosternum und an den Labellen vonCalliphora erythrocephala Mg (Diptera). Z Morphol ökol Tiere 51:211–226Google Scholar
  49. Pflüger H-J, Tautz J (1982) Air movement sensitive hairs and interneurons inLocusta migratoria. J Comp Physiol 145:369–380Google Scholar
  50. Pflugstaedt H (1912) Die Halteren der Dipteren. Z Wiss Zool 100:1–59Google Scholar
  51. Pringle JWS (1948) The gyroscopic mechanism of the halteres of Diptera. Phil Trans R Soc Lond B 233:347–384Google Scholar
  52. Robinson DA (1981) Control of eye movements. In: Brookhart JM, Mountcastle VB (eds) Handbook of physiology. I: The nervous system, pp 1275–1320Google Scholar
  53. Sakaguchi DS, Murphey RK (1983) The equilibrium detecting system of the cricket: physiology and morphology of an identified interneuron. J Comp Physiol 150:141–152Google Scholar
  54. Sandeman DC (1980) Angular acceleration, compensatory head movements and the halteres of flies (Lucilia serricata). J Comp Physiol 136:361–367Google Scholar
  55. Sandeman DC (1983) The balance and visual systems of the swimming crab: their morphology and interaction. In: Horn E (ed) Multimodal convergences in sensory systems. Fortschr Zool 28:213–230Google Scholar
  56. Sandeman DC, Markl H (1980) Head movements in flies (Calliphora) produced by deflexion of the halteres. J Exp Biol 85:43–60Google Scholar
  57. Schmidt-Koenig K (1975) Migration and homing in animals. Zoophysiology and ecology, vol 6. Springer, Berlin Heidelberg New YorkGoogle Scholar
  58. Schneider G (1953) Die Halteren der Schmeißfliege (Calliphora) als Sinnesorgane und als mechanische Flugstabilisatoren. Z Vergl Physiol 35:416–458Google Scholar
  59. Shepard RN, Cooper LA (1982) Mental images and their transformations. MIT Press, Bradford Books, Cambridge, MassGoogle Scholar
  60. Sihler H (1924) Die Sinnesorgane an den Cerci der Insekten. Zool Jb Abt Anat Ontog 45:519–580Google Scholar
  61. Srinivasan MV (1977) A visually evoked roll response of the houseflyMusca. J Comp Physiol 119:1–14Google Scholar
  62. Stedtler A (1974) Die Repräsentation von Schwingungen der Fliegenhaltere in den Reaktionen ihrer Mechanorezeptor-Felder. Staatsexamens-Arbeit, Universität BochumGoogle Scholar
  63. Strausfeld NJ, Seyan HS (1985) Convergence of visual, haltere, and prosternal inputs at neck motor neurons ofCalliphora erythrocephala. Cell Tissue Res 240:601–615Google Scholar
  64. Strausfeld NJ, Seyan HS, Milde JJ (1987) The neck motor system of the flyCalliphora erythrocephala. I. Muscles and motor neurons. J Comp Physiol A 160:205–224Google Scholar
  65. Thurm U, Stedtler A, Foelix R (1974) Reizwirksame Verformungen der Terminalstrukturen eines Mechanorezeptors. Verh Dtsch Zool Ges 67:37–41Google Scholar
  66. Tracey D (1975) Head movements mediated by halteres in the fly,Musca domestica. Experientia 31:44–45Google Scholar
  67. Vater G (1961) Vergleichende Untersuchungen über die Morphologie des Nervensystems der Dipteren. Z Wiss Zool 167:137–196Google Scholar
  68. Wehner R (1967) Zur Physiologie des Formensehens bei der Honigbiene. II. Winkelunterscheidung an Streifenmustern bei variabler Lage der Musterebene im Schwerefeld. Z Vergl Physiol 55:145–166Google Scholar
  69. Wehner R (1981) Spatial vision in arthropods. In: Autrum H (ed) Handbook of sensory physiology, vol VII/6c. Springer, Berlin Heidelberg New York, pp 287–616Google Scholar
  70. Weismann A (1863) über die Entstehung des vollendeten Insekts in Larve und Puppe. Senckenbergische naturf. Gesellsch., FrankfurtGoogle Scholar
  71. Wendler G (1974) The influence of proprioceptive feedback on locust flight coordination. J Comp Physiol 88:173–200Google Scholar
  72. Zaćwilichowski J (1931) über die Innervierung und die Sinnesorgane der Flügel der Insekten. Bull Acad Pol Chl Math Nat I. II. 391–424Google Scholar
  73. Zill SN, Moran DT (1981) The exoskeleton and insect proprioception: I. Responses of tibial campaniform sensilla to external and muscle-generated forces in the American cockroach,Periplaneta americana. J Exp Biol 91:1–24Google Scholar

Copyright information

© Springer-Verlag 1988

Authors and Affiliations

  • Roland Hengstenberg
    • 1
  1. 1.Max-Planck-Institut für biologische KybernetikTübingenFederal Republic of Germany

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