Skip to main content
Log in

The flight maintenance mechanism in the cockroachPeriplaneta americana L.

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

Summary

  1. 1.

    In order to find the receptors that maintained flight in the cockroachPeriplaneta americana a wind tunnel was used (Fig. 1A).

  2. 2.

    After removal of the antennal flagella prolonged flight was not possible. However, sticking of cut antenna restored flight capability (Table 2a, b). These data showed that for maintenance of cockroach flight antennal flagella were needed as levers acting on pedicel receptors: chordotonal sensilla (including the chordotonal sensilla of Johnston's organ) and sensilla campaniformia.

  3. 3.

    In the laminar airstream passive antennal vibration caused by the wing motor activity was absent and the observed antennal movements in flight were evoked only by antennal muscle activity. Fixation of active antennal movements by immobilization the head-scapus and scapus-pedicel joints leads to cessation of flight. Therefore, pedicel receptors are capable to maintain the cockroach flight only if active antennal movements in the airstream are present.

  4. 4.

    The frequency of active antennal movements with amplitude of more than 1 mm is in the cause of 3–10 Hz (Fig. 3B). Each of these active movements like at instantaneous cessation of\(\bar 1\) 1 and\(\overline 1 \overline 1 \) 1 antennal joints evoked lash (passive deflection) of its flagellum relatively to the pedicel. To estimate low-amplitude passive deflexions which are defined by high-amplitude active movements due to the inertia, ‘sail-property’ and weight of the flagellum a mathematical model was developed. This model describes the displacements of the cockroach flagellum which are evoked by the active movements in the airstream of different velocity.

  5. 5.

    The application of the constructed mathematical model showed that at active antennal movements in the air current velocity of 1.5–2 m/s (minimum velocity at which the cockroach flight was possible) the angle determined by the flagellum weight (its ‘sagging’) was compensated and the angle of flagellum displacement relative to the pedicel at the active movements upward was increased by 1.5–2 times as compared with the same angles at the same antennal movements in still air (Fig. 4). It seems clear that just the redistribution of the load on the pedicel receptors was that mechanical stimulus which periodically acting with frequency of active antennal movements of 3–10 Hz led to alterate the mosaic of excitation of differently located in pedicel chordotonal and campaniform sensilla (functional asymmetry of the system of pedicel receptors) and ultimate maintenance of prolonged flight.

  6. 6.

    Microelectrode recording of electrical activity of the pedicel sensilla showed that three functional types of receptors (phasic-tonic receptors with slow and incomplete adaptation, phasic-tonic receptors with fast and complete adaptation and phasic receptors) were revealed. These receptors perceived the changes in amplitude (starting from 20–30 μm), the frequency (up to 50 Hz, Fig. 6), the flagellum movement velocity as well as they had directional sensitivity. (The sector of the maximal sensitivity was 90–135° in most receptors.) Thus, redistribution of the load in flight from the ventral to dorsal side of the pedicel evoked electrical activity of a definite group of receptors. The sectors of maximal sensitivity of these receptors were dorsally orientated.

  7. 7.

    The pedicel mechanoreceptors' responses in the cockroach head ganglia went over into the descending interneurons of three functional types including the phasic-tonic type with slow incomplete adaptation, the phasic-tonic type with fast and complete adaptation and phasic interneurons. In the cockroach brain the chiasma of the nervous tracts provides receiving the information about the flagellum deflexion to the left and right sides of the prothoracic ganglia. Interneurons were not able to respond for a long time to flagellum vibration, if its frequency exceeded 10 Hz (Fig. 8). Thus, it was evident that electrical activity maintaining the cockroach flight consisted of the impulse bursts of the pedicel receptors and related interneurons at each deflection of the flagellum with regard to the pedicel at the active antennal movements in the air current.

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.

Institutional subscriptions

Similar content being viewed by others

References

  • Akita K (1979) Flight activity of the mothTonglia fischeri. New Entomol 28:63–69

    Google Scholar 

  • Bässler U (1958) Versuche zur Orientierung der Stechmücken: Die Schwarmbildung und die Bedeutung des Johnstonschen Organs. Z Vergl Physiol 41:300–330

    Google Scholar 

  • Burkhardt D, Gewecke M (1965) Mechanoreception in Arthropoda: the chain from stimulus to behavioral pattern. Cold Spring Harbor Symp Quant Biol 30:601–614

    Google Scholar 

  • Burkhardt D, Schneider G (1957) Die Antennen vonCalliphora als Anzeiger der Fluggeschwindigkeit. Z Naturforsch 12b:139–143

    Google Scholar 

  • Burrows M (1973) The role of delayed excitation in the coordination of some metathoracic flight motoneurons of a locust. J Comp Physiol 83:135–164

    Google Scholar 

  • Camhi JM (1969a) Locust wind receptors. I. Transducer mechanics and sensory response. J Exp Biol 50:335–348

    Google Scholar 

  • Camhi JM (1969b) Locust wind receptors. II. Interneurons in the cervical connective. J Exp Biol 50:349–362

    Google Scholar 

  • Diakonoff A (1936) Contribution to the knowledge of the fly reflexes and the static sense inPeriplaneta americana. L. Arch Neerl Physiol 21:104–129

    Google Scholar 

  • Fraenkel C (1932) Untersuchungen über die Koordination von Reflexen und automatisch-nervösen Rhythmen bei Insekten. I. Die Flugreflexe der Insekten und ihre Koordination. Z Vergl Physiol 16:371–393

    Google Scholar 

  • Gewecke M (1967) Die Wirkung von Luftströmung auf die Antennen und das Flugverhalten der Blauen Schmeissfliege (Calliphora erythrocephala). Z Vergl Physiol 54:121–164

    Google Scholar 

  • Gewecke M (1970) Antennae: another wind-sensitive receptor in locusts. Nature 225:1263–1264

    Google Scholar 

  • Gewecke M (1972) Antennen und Stirn-Scheitelhaare vonLocusta migratoria L. als Luftströmungs-Sinnesorgane bei der Flugsteuerung. J Comp Physiol 80:57–94

    Google Scholar 

  • Gewecke M (1974) The antennae of insects as air-current sense organs and their relationship to the control of flight. In: Barton Browne L (ed) Experimental analysis of insect behaviour. Springer, Berlin Heidelberg New York, pp 100–113

    Google Scholar 

  • Gewecke M (1975) The influence of the air-current sense organs on the flight behaviour ofLocusta migratoria. J Comp Physiol 103:79–95

    Google Scholar 

  • Gewecke M (1979) Central projection of antennal afferents for the flight motor inLocusta migratoria (Orthoptera: Acrididae). Entomol Gen 5:317–320

    Google Scholar 

  • Gewecke M, Heinzel H-G, Philippen J (1974) Role of antennae of the dragonflyOrthetrum cancellatum in flight control. Nature 249:584–585

    Google Scholar 

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

    Google Scholar 

  • Gewecke M, Schlegel P (1970) Die Schwingungen der Antenne und ihre Bedeutung für die Flugsteuerung beiCalliphora erythrocephala. Z Vergl Physiol 67:325–362

    Google Scholar 

  • Guthrie DH, Tindall AR (1968) The biology of cockroach. Beccles, Arnold, London

    Google Scholar 

  • Haskell PT (1958) Physiology of some wind sensitive receptors of the desert locust (Schistocerca gregaria). Abstr XV Zool Congr London 15:960

    Google Scholar 

  • Heran H (1959) Wahrnehmung und Regelung der Flugeigengeschwindigkeit beiApis mellifica L. Z Vergl Physiol 42:103–163

    Google Scholar 

  • Hollick FSJ (1940) The flight of the dipterous flyMuscina stabulans Fallen. J Phil Trans R Soc Lond B 230:357–390

    Google Scholar 

  • Johnson B (1956) Function of the antennae of aphids during flight. Austr J Sci 18:199–200

    Google Scholar 

  • Karelin YA (1978) Electron microscopic investigation of the receptive fields of the head which maintain the flight inLocusta migratoria. In: Kreps FM (ed) Morphological bases of functional evolution, Leningrad, Nauka, pp 30–34

    Google Scholar 

  • Karelin YA, Voronina W, Kublanova IK, Svidersky VL (1976) Functional peculiarities of wind-sensitive receptors triggering the activity of wing muscle neurons inCalliptanus barbarus. J Evol Biochem Physiol 12:44–50

    Google Scholar 

  • Krämer K, Markl M (1978) Flight-inhibition on ground contact in the American cockroach,Periplaneta americana. I. Contact receptors and a model for their central connections. J Insect Physiol 24:577–586

    Google Scholar 

  • Lambin M (1973) Les sensilles de l'antenne chez quelques blattes et en particulier chezBlaberus craniifer (Burm). Z Zellforsch 143:183–206

    Google Scholar 

  • Lorenz KZ (1950) The comparative method in studying innate behavior patterns. Symp Soc Exp Biol 4:221–268

    Google Scholar 

  • Petryszak A (1975) The sensory peripheral nervous system ofPeriplaneta americana (L.) (Blattodea). Part 11. Antenna. Acta Biol Crac Zool XVIII: 257–263

    Google Scholar 

  • Pringle JWA (1938) Proprioception in insects. J Exp Biol 15:101–132

    Google Scholar 

  • Shorey HH (1964) Sex pheromones of noctuid moths. Ann Entomol Soc Am 57:371–377

    Google Scholar 

  • Smola U (1970) Untersuchung zur Topographie, Mechanik und Strömungsmechanik der Sinneshaare auf dem Kopf der WanderheuschreckeLocusta migratoria. Z Vergl Physiol 67:382–402

    Google Scholar 

  • Sveshnikoff VG (1970) Reflex mechanisms initiating and maintaining the flight of the dragonflyAeschna grandis. J Evol Biochem Physiol 6:472–473

    Google Scholar 

  • Sveshnikoff VG (1972) The structure and functional peculiarities of the head receptors controlling the activity of wing muscles in the dragonflyAeschna grandis. J Evol Biochem Physiol 8:530–535

    Google Scholar 

  • Svidersky VL (1967) Electrical activity of the receptors which maintain the locust flight. Dokl Acad Nauk USSR 172:1230–1234

    Google Scholar 

  • Svidersky VL (1968) Functional neuron organization providing activity of wing muscles inLocusta migratoria. Proc XIII Int Congr Entomol Moscow 2:41–42

    Google Scholar 

  • Svidersky VL (1969a) Nervous control of the fast rhythmic contractions of the insect muscles (Cicada sound-production apparatus, locust wing motor). In: Actual problems of the insect nervous system structure and function. Transact All-Union Entomol Soc Nauka 53:91–131

    Google Scholar 

  • Svidersky VL (1969b) Receptors of the forehead of the locust,Locusta migratoria in ontogenesis. J Evol Biochem Physiol 5:482–490

    Google Scholar 

  • Svidersky VL (1973) The neurophysiology of insect flight. Leningrad, Nauka

    Google Scholar 

  • Weis-Fogh T (1949) An aerodynamic sense organ stimulating and regulating flight in locusts. Nature 164:873–874

    Google Scholar 

  • Weis-Fogh T (1956) Biology and physics of locust flight. IV. Notes on sensory mechanisms in locust flight. Phil Trans R Soc Lond B 239:553–584

    Google Scholar 

  • Wilson DM (1961) The central nervous control of flight in locust. J Exp Biol 38:471–490

    Google Scholar 

  • Wilson DM (1968) The nervous control of insect flight and related behaviour. Adv Insect Physiol 5:289–338

    Google Scholar 

  • Yagodin SV (1979a) Photoperiodic regulation of circadian rhythms inBarathra brassicae. Vestn Leningr Univ 3:48–54

    Google Scholar 

  • Yagodin SV (1979b) Localization of the receptors which provide for initiation and maintenance of the flight in the cockroachPeriplaneta americana. J Evol Biochem Physiol 15:576–582

    Google Scholar 

  • Yagodin SV (1980a) The role of the antenna in maintenance of the flight in the cockroachPeriplaneta americana. J Evol Biochem Physiol 16:39–46

    Google Scholar 

  • Yagodin SV (1980b) The relationship of flight duration in the cockroachPeriplaneta americana to temperature, air humidity and daytime. J Evol Biochem Physiol 16:314–317

    Google Scholar 

  • Yagodin SV (1981) Functional properties of the cockroachPeriplaneta americana (Blattodea) antennal receptors with reference to the maintenance of the prolonged flight. Entomol Obozr 60:511–522

    Google Scholar 

  • Yagodin SV, Svidersky VL (1980a) The directional sensitivity of pedicel receptors in cockroachPeriplaneta americana. J Evol Biochem Physiol 16:529–532

    Google Scholar 

  • Yagodin SV, Svidersky VL (1980b) Functional peculiarities of the receptors which maintain the cockroachPeriplaneta americana flight. Dokl Acad Nauk USSR 250:1277–1280

    Google Scholar 

  • Yagodin SV, Svidersky VL (1983) Central transformation of the maintained cockroachPeriplaneta americana flight afferent impulsation. Dokl Acad Nauk USSR 268:506–509

    Google Scholar 

  • Yagodin SV, Svidersky VL, Kovbasa SI (1983) Mathematical model and analysis of flight maintenance mechanism in the cockroachPeriplaneta americana. J Evol Biochem Physiol 19:46–53

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yagodin, S.V., Kovbasa, S.I. The flight maintenance mechanism in the cockroachPeriplaneta americana L.. J. Comp. Physiol. 155, 697–712 (1984). https://doi.org/10.1007/BF00610856

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00610856

Keywords

Navigation