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The influence of head position on the flight behaviour of the fly. Calliphora erythrocephala
J. Insect Physiol., 1977, Vol. 23. pp. 375 ro 379. Pergamon Press. Printed in Great Britain.
THE INFLUENCE OF HEAD POSITION ON THE FLIGHT BEHAVIOUR OF THE FLY.
CALLIPHORA ERYTHROCEPHALA* ECKEHARDLIXE Zoologisches Institut der Technischen Hochschule Darmstadt, Schnittspahnstrabe D-6100 Darmstadt, Federal Republic of Germany
3,
(Received 4 September 1976) Abstract-The heads of flies were passively turned during fixed flight (open loop conditions). The turning stimuli had ramp-shaped onsets. The resulting torque produced by the thorax was plotted as a function of the degree of head-turn. Directional, passive turns of the head evoke active turning tendencies (yawing forces) of the same sign from the thorax. The strength of these tendencies is dependent on the size of the given angle through which the head was turned. The cushion of sensory hairs on the neck (prostemal organ) is very important in the elicitation of the turning tendencies. The results which have been obtained indicate that the position of the fly’s head has a substantial influence on the magnitude of the turning tendencies elicited by visual stimuli.
INTRODUCI’ION MITI-EL-STAEDT (1950) has shown that in the dragonfly Anax imperator passive rotation of the head elicits active body rotation which has the same sign. He observed the rolling movements (rotation about the longitudinal axis) of the head and thorax which his experimental animals performed during tethered flight. In the blowfly. Calliphora erythrocephala, LAND (1973, 1975) found that active head movements are also followed by body turns which have the same direction. LAND studied turning movements (rotation about the dorso-ventral axis) of the head and body during tethered flight. The work presented here is the first quantitative analysis of the relationship between head and body turning in flying insects. A further aim of these experiments is to elucidate the influence of head position on body rotations which are elicited by visual stimuli. MATERIAL
AND METHODS
Calliphora females were fixed at the thorax to an electronic torque meter. The torque of the flies about the dorso-ventral body axis represents a characteristic index of tethered flight which can be continuously registered. The turns which the flies made never * I would like to thank Dr. W. KAISERfor much critical and fruitful discussion and Mr. DEUSER,Staatliche Materialpriifungsanstalt. Darmstadt. for help with the use of the scanning electronmicroscope. Further. I wish to thank Mrs. J. STEINER-KAISER for translating the manuscript. This work was supported by the Deutsche Forschungsgemeinschaft.
deviated by more than 0.1” from zero when they were attached to the torque meter. The fly’s head, in its normal position, was attached between the compound eyes to the lower end of a rotatable shaft. This was itself perpendicular to the longitudinal body axis as well as being vertical in space. The upper end of the shaft was connected to ;t loudspeaker or an electromagnet by means of a lever system. The fly’s head was thus turned passively. with a ramp-shaped onset of the turning movement, always starting from the same resting position (in which the longitudinal axes of head and body coincide). The rotating shaft turned the head through different angles (degree of turning. e) with variable rise times (50msec and 1 set). For each 8. the Ry’s head was turned consecutively first to the right, 7 to 10 times and then to the left, also 7 to 10 times. The head returned to the resting position between each individual turn. The torque produced by the thorax for each turn of the head was summated over 2 sec. This integration process was triggered just before the head reached its ultimate position. It was necessary to integrate over 2sec and to calculate the average values for 7 to 10 individual integration values in order to compensate for the considerable spontaneous fluctuations of the fly’s torque. The integration process and calculation of average values was performed with an Interdata M-70 computer which also eliminated the torque which was transmitted to the thorax during head turning because of the elastic junction between head and thorax.
375
ECHEHARD LISKE
376
All experiments were performed in total darkness
tive function. I have made the first scanning electron-
in order to eliminate any influence of visual stimuli
microscope study of this organ (Fig. 2). An experimental series was carried out in which the prosternal organ was plastered over. It is probable that the sensory hairs were permanently and non-specifically stimulated due to this operation. As a result of this procedure. it was no longer possible to elicit specific body-torque when the head was passively turned: the average of the stimulus responses from all animals fluctuated around zero. However, some animals do demonstrate non-specific turning tendencies which are independent of the position of the head.
on the turning tendencies. RESULTS Directional, passive turns of the head induce from the thorax active turning tendencies having the same sign (Fig. 1). The size of the torque is proportional to the degree of the head turn. This is true up to an angle of approximately 8’. If the angle is larger. the reaction probably approaches a saturation value. (Rapid. active head turns (saccades) reach amplitudes up to approximately 20’ in Calliphora (LAND, 1975)). The course of the reaction characteristic is virtually symmetrical for head movements to the right and to the left. The specific torque for a particular, maintained head position remains stable for quite a long time (see Fig. 1). Turning of the head alone is a much less effective stimulus for Calliphora than a strong visual stimulus. Control experiments have, in fact, demonstrated that a moving black-and-white striped pattern elicits turning tendencies which are on the average, three times larger than the maximal torque which can be induced by a 15’ passive turning of the head. Since all experiments were performed in total darkness, the only possible factor which can elicit turning tendencies must be the stimulation of a mechanoreceptive sense organ. A conspicuous cushion of sensory hairs on the neck of these flies, the prostemal organ (PETERS,1962), probably possesses a mechanorecep-
DISCUSSION It is very likely that the active turning tendencies of the body which are elicited by turning of the head enable flies to annul, in flight, differences between the longitudinal axes of head and body. The prosternal organ participates to a large extent in the evocation of these turning tendencies. The actual contribution of this sense organ can only be unequivocally demonstrated in neural isolation experiments in which its nerve is severed. Earlier behavioural investigations involving isolation experiments in flying dragonflies (MITTELSTAEDT,1950) and flying locusts (GOODMAN, 1965) demonstrated that the neck receptor system plays a definitive role in the co-ordination of head and body movements. It might, however, also be possible that, in addition to the prosternal organ, other mechanoreceptive sense organs such as the antennae (GEWECKE, 1967) and/or the prothoracic
Head position Bldcg)
Left f
Fig. 1. Normaliied reaction (torque) of fixed hying flies in response to passive ramp-shaped head-tuming through different turning angles 8. A-A, average of four curves from four different animals. Rise time for head turn 1 sec. @---O. average of two curves from two different animals. Rise time SOmsec. For technical reasons it was only possible to produce head turns to the right. q---Xl. the fly’s head was turned through a particular angle and then fixed rigidly to the thorax. Five minutes later. the torque elicited from the thorax was registered for 3.5 min and averaged. One curve from one fly. The vertical bars represent the standard deviation of the mean (+ sy).
377
Fig. 2. Prostemal organ of Calliphora erythrocephala. Scanning electronmicroscope, scale: 50 pm. A hairless zone divides the prosternal organ into right and left halves. The sensory hairs are situated on prolongations of the prostemum (Ps). When the head turns, the so-called contact piece-s (C), which are cuticular structures on the skin of the neck, move in such a way that they cause the hairs to bend.
Flight behaviour of the fly, Calliphora erythrocephala chordotonal organs (VATER,1961) are involved in this reaction. although to a lesser extent. However, none of the experiments which I have undertaken to date, using flies without antennae, have provided an indication of the participation of the antennae under these experimental conditions. The isolation experiments mentioned earlier should also provide information about the possible role of the prothoracic chordotonal organs. My attention is now focussed on the following problem: what influence does the position of the fly’s head have on the torque which is elicited by visual stimuli? Experiments performed so far using moving visual stimuli and flies whose heads had been turned through a particular angle prior to visual stimulation have demonstrated that both sensory systems interact with one another in determining the magnitude of the turning tendencies. Perhaps this kind of experiment will be able to throw light on the type of
mechanism which the flv uses to differentiate between image movements
over-its
retina
caused
by its own
head movement and those due to movement external
visual environment.
of the
379
REFERENCES GE~ECKEM. (1967) Die Wirkung von Luftstramung
auf die Antennen und das Fluaverhalten der BIauen Schmeissfiege (Calfiphora eryth;ocephala). 2. cergl. Phvsiol. 54, 121-164. GOODMANL. J. (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. LAND M. F. (1973) Head movements of flies during visually guided flight. Nature, Lond. 243. 299-300. LAND M. F. (1975) Head movements and Hy vision. In The Compound Eye and Vision of Insects (Ed. by HORRIDGEG. A.). pp. 469189. Clarendon Press. Oxford
MIITELSTAEDT H. (1950) Physiologie des Gleichgewichtssinnes bei fliegenden Libellen. 2. cergl. Physiol. 32. 422-463. PETERSW. (1962) Die propriorezeptiven Organe am Prosternum und an den Labellen vr+n Calliphorn erythrocephala Mg. (Diptera). Z. Morph. Okol. Tiere 51, 211-226. VATER G. (1961) Vergleichende Untersuchungen fiber die Morphologie des Nervensystems der Dipteren. Z. wiss. Zool. 167. 137-196.
THE INFLUENCE OF HEAD POSITION ON THE FLIGHT BEHAVIOUR OF THE FLY.
CALLIPHORA ERYTHROCEPHALA* ECKEHARDLIXE Zoologisches Institut der Technischen Hochschule Darmstadt, Schnittspahnstrabe D-6100 Darmstadt, Federal Republic of Germany
3,
(Received 4 September 1976) Abstract-The heads of flies were passively turned during fixed flight (open loop conditions). The turning stimuli had ramp-shaped onsets. The resulting torque produced by the thorax was plotted as a function of the degree of head-turn. Directional, passive turns of the head evoke active turning tendencies (yawing forces) of the same sign from the thorax. The strength of these tendencies is dependent on the size of the given angle through which the head was turned. The cushion of sensory hairs on the neck (prostemal organ) is very important in the elicitation of the turning tendencies. The results which have been obtained indicate that the position of the fly’s head has a substantial influence on the magnitude of the turning tendencies elicited by visual stimuli.
INTRODUCI’ION MITI-EL-STAEDT (1950) has shown that in the dragonfly Anax imperator passive rotation of the head elicits active body rotation which has the same sign. He observed the rolling movements (rotation about the longitudinal axis) of the head and thorax which his experimental animals performed during tethered flight. In the blowfly. Calliphora erythrocephala, LAND (1973, 1975) found that active head movements are also followed by body turns which have the same direction. LAND studied turning movements (rotation about the dorso-ventral axis) of the head and body during tethered flight. The work presented here is the first quantitative analysis of the relationship between head and body turning in flying insects. A further aim of these experiments is to elucidate the influence of head position on body rotations which are elicited by visual stimuli. MATERIAL
AND METHODS
Calliphora females were fixed at the thorax to an electronic torque meter. The torque of the flies about the dorso-ventral body axis represents a characteristic index of tethered flight which can be continuously registered. The turns which the flies made never * I would like to thank Dr. W. KAISERfor much critical and fruitful discussion and Mr. DEUSER,Staatliche Materialpriifungsanstalt. Darmstadt. for help with the use of the scanning electronmicroscope. Further. I wish to thank Mrs. J. STEINER-KAISER for translating the manuscript. This work was supported by the Deutsche Forschungsgemeinschaft.
deviated by more than 0.1” from zero when they were attached to the torque meter. The fly’s head, in its normal position, was attached between the compound eyes to the lower end of a rotatable shaft. This was itself perpendicular to the longitudinal body axis as well as being vertical in space. The upper end of the shaft was connected to ;t loudspeaker or an electromagnet by means of a lever system. The fly’s head was thus turned passively. with a ramp-shaped onset of the turning movement, always starting from the same resting position (in which the longitudinal axes of head and body coincide). The rotating shaft turned the head through different angles (degree of turning. e) with variable rise times (50msec and 1 set). For each 8. the Ry’s head was turned consecutively first to the right, 7 to 10 times and then to the left, also 7 to 10 times. The head returned to the resting position between each individual turn. The torque produced by the thorax for each turn of the head was summated over 2 sec. This integration process was triggered just before the head reached its ultimate position. It was necessary to integrate over 2sec and to calculate the average values for 7 to 10 individual integration values in order to compensate for the considerable spontaneous fluctuations of the fly’s torque. The integration process and calculation of average values was performed with an Interdata M-70 computer which also eliminated the torque which was transmitted to the thorax during head turning because of the elastic junction between head and thorax.
375
ECHEHARD LISKE
376
All experiments were performed in total darkness
tive function. I have made the first scanning electron-
in order to eliminate any influence of visual stimuli
microscope study of this organ (Fig. 2). An experimental series was carried out in which the prosternal organ was plastered over. It is probable that the sensory hairs were permanently and non-specifically stimulated due to this operation. As a result of this procedure. it was no longer possible to elicit specific body-torque when the head was passively turned: the average of the stimulus responses from all animals fluctuated around zero. However, some animals do demonstrate non-specific turning tendencies which are independent of the position of the head.
on the turning tendencies. RESULTS Directional, passive turns of the head induce from the thorax active turning tendencies having the same sign (Fig. 1). The size of the torque is proportional to the degree of the head turn. This is true up to an angle of approximately 8’. If the angle is larger. the reaction probably approaches a saturation value. (Rapid. active head turns (saccades) reach amplitudes up to approximately 20’ in Calliphora (LAND, 1975)). The course of the reaction characteristic is virtually symmetrical for head movements to the right and to the left. The specific torque for a particular, maintained head position remains stable for quite a long time (see Fig. 1). Turning of the head alone is a much less effective stimulus for Calliphora than a strong visual stimulus. Control experiments have, in fact, demonstrated that a moving black-and-white striped pattern elicits turning tendencies which are on the average, three times larger than the maximal torque which can be induced by a 15’ passive turning of the head. Since all experiments were performed in total darkness, the only possible factor which can elicit turning tendencies must be the stimulation of a mechanoreceptive sense organ. A conspicuous cushion of sensory hairs on the neck of these flies, the prostemal organ (PETERS,1962), probably possesses a mechanorecep-
DISCUSSION It is very likely that the active turning tendencies of the body which are elicited by turning of the head enable flies to annul, in flight, differences between the longitudinal axes of head and body. The prosternal organ participates to a large extent in the evocation of these turning tendencies. The actual contribution of this sense organ can only be unequivocally demonstrated in neural isolation experiments in which its nerve is severed. Earlier behavioural investigations involving isolation experiments in flying dragonflies (MITTELSTAEDT,1950) and flying locusts (GOODMAN, 1965) demonstrated that the neck receptor system plays a definitive role in the co-ordination of head and body movements. It might, however, also be possible that, in addition to the prosternal organ, other mechanoreceptive sense organs such as the antennae (GEWECKE, 1967) and/or the prothoracic
Head position Bldcg)
Left f
Fig. 1. Normaliied reaction (torque) of fixed hying flies in response to passive ramp-shaped head-tuming through different turning angles 8. A-A, average of four curves from four different animals. Rise time for head turn 1 sec. @---O. average of two curves from two different animals. Rise time SOmsec. For technical reasons it was only possible to produce head turns to the right. q---Xl. the fly’s head was turned through a particular angle and then fixed rigidly to the thorax. Five minutes later. the torque elicited from the thorax was registered for 3.5 min and averaged. One curve from one fly. The vertical bars represent the standard deviation of the mean (+ sy).
377
Fig. 2. Prostemal organ of Calliphora erythrocephala. Scanning electronmicroscope, scale: 50 pm. A hairless zone divides the prosternal organ into right and left halves. The sensory hairs are situated on prolongations of the prostemum (Ps). When the head turns, the so-called contact piece-s (C), which are cuticular structures on the skin of the neck, move in such a way that they cause the hairs to bend.
Flight behaviour of the fly, Calliphora erythrocephala chordotonal organs (VATER,1961) are involved in this reaction. although to a lesser extent. However, none of the experiments which I have undertaken to date, using flies without antennae, have provided an indication of the participation of the antennae under these experimental conditions. The isolation experiments mentioned earlier should also provide information about the possible role of the prothoracic chordotonal organs. My attention is now focussed on the following problem: what influence does the position of the fly’s head have on the torque which is elicited by visual stimuli? Experiments performed so far using moving visual stimuli and flies whose heads had been turned through a particular angle prior to visual stimulation have demonstrated that both sensory systems interact with one another in determining the magnitude of the turning tendencies. Perhaps this kind of experiment will be able to throw light on the type of
mechanism which the flv uses to differentiate between image movements
over-its
retina
caused
by its own
head movement and those due to movement external
visual environment.
of the
379
REFERENCES GE~ECKEM. (1967) Die Wirkung von Luftstramung
auf die Antennen und das Fluaverhalten der BIauen Schmeissfiege (Calfiphora eryth;ocephala). 2. cergl. Phvsiol. 54, 121-164. GOODMANL. J. (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. LAND M. F. (1973) Head movements of flies during visually guided flight. Nature, Lond. 243. 299-300. LAND M. F. (1975) Head movements and Hy vision. In The Compound Eye and Vision of Insects (Ed. by HORRIDGEG. A.). pp. 469189. Clarendon Press. Oxford
MIITELSTAEDT H. (1950) Physiologie des Gleichgewichtssinnes bei fliegenden Libellen. 2. cergl. Physiol. 32. 422-463. PETERSW. (1962) Die propriorezeptiven Organe am Prosternum und an den Labellen vr+n Calliphorn erythrocephala Mg. (Diptera). Z. Morph. Okol. Tiere 51, 211-226. VATER G. (1961) Vergleichende Untersuchungen fiber die Morphologie des Nervensystems der Dipteren. Z. wiss. Zool. 167. 137-196.