Abstract
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1)
A standing cockroach (Periplaneta americana) responds to the air displacement made by an approaching predator, by turning away and running. The wind receptors on the cerci, two posterior sensory appendages, excite a group of ventral giant interneurons that mediate this response. While flying, these interneurons remain silent, owing to strong inhibition; however, the dorsal giant interneurons respond strongly to wind. Using behavioral and electromyographic analysis, we sought to determine whether flying cockroaches also turn away from air displacement like that produced by an approaching flying predator; and if so, whether the cerci and dorsal giant interneurons mediate this response.
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2)
When presented with a wind puff from the side, a flying cockroach carries out a variety of maneuvers that would cause a rapid turn away and perhaps a dive. These are not evoked if the cerci are ablated (Figs. 4, 5, 6).
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3)
This evasive response appears to be mediated by a circuit separate from that mediating escape when the cockroach is standing (Fig. 7).
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4)
The dorsal giant interneurons respond during flight in a directional manner that is suited to mediate this behavior (Fig. 8).
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5)
Recordings of the wind produced by a moving model predator (Fig. 9), together with measurements of the behavioral latency of tethered cockroaches, suggest that the evasive response would begin just milliseconds before a predator actually arrives. However, as explained in the Discussion section, under natural conditions, the evasive response may well begin earlier, and could indeed be useful in escaping from predators.
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6)
If cockroaches had a wind-mediated yaw-correcting behavior, as locusts have, this could conflict with the wind-evoked escape. In fact, cockroaches show the opposite, yaw-enhancing response, mediated by the cerci, that does not present a conflict with escape (Figs. 10–14).
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to check access.Abbreviations
- GI:
-
giant interneuron
- vGI:
-
ventral giant interneuron
- dGI:
-
dorsal giant interneuron
- EMG:
-
electromyogram
- T1, T2, T3:
-
first, second, third thoracic segment
- CF:
-
coxo-femoral
References
Altman J (1982) Sensory inputs and the generation of the locust flight motor pattern: From the past to the future. In: Nachtigall W (ed) Insect Flight. Biona Report, G Fischer, Stuttgart, pp 127–136
Arbas E A (1986) Control of hindlimb posture by wind sensitive hairs and antennae during locust flight. J Comp Physiol A 159: 849–857
Baader A (1990) The posture of the abdomen during locust flight: Regulation by steering and ventilatory interneurons. J Exp Biol 151: 109–131
Baker PS (1979) The wing movements of flying locusts during steering behavior. J Comp Physiol 131: 49–58
Baronetsky BE, Möhl B (1987) Afferent input from the cerci on the locust flight motor. In: Elsner N, Creutzfeld O (eds) New frontiers in brain research: Proc 15th Göttingen Neurobiol Conf. G. Thieme, Stuttgart, p 50
Boyan GS, Ball EE (1989) The wind-sensitive cercal receptor/giant interneurone system of the locust, Locusta migratoria. III. Cereal activation of thoracic motor pathways. J Comp Physiol A 165: 523–537
Boyan GS, Ball EE (1990) Neural organization and information processing in the wind-sensitive cereal receptor/giant interneuron system of the locust and other orthopteroid insects. Prog Neurobiol 35: 217–243
Callec JJ, Satelle P (1973) A simple technique for monitoring the synaptic actions of pharmacological agents. J Exp Biol 59: 725–738
Camhi JM (1970) Yaw-correcting postural changes in locusts. J Exp Biol 52: 533–537
Camhi JM (1993) Neural mechanisms of behavior. Current Opinion Neurobiol 3: 1011–1019
Camhi JM, Levy A (1989) The code for stimulus direction in a cell assembly in the cockroach. J Comp Physiol A 165: 83–97
Camhi JM, Levy A (1988) Organization of complex movement: fixed and variable components of the cockroach escape behavior. J Comp Physiol A 163: 317–328
Comer CM (1985) Analyzing cockroach escape behavior with lesions of individual giant interneurons. Brain Res 335: 342–346
Comer CM (1993) Multisensory processing for movement: Antennal and cereal mediation of escape turning in the cockroach. In: Beer RD, Ritzmann RE, McKenna T (eds) Biological neural networks in invertebrate neuroethology and robotics. Academic Press, New York, pp 89–112
Dambach M, Rausche H-G, Wendler G (1983) Proprioceptive feedback influences the calling song of the field cricket. Naturwissenschaften 70: 417–418
Dugard JJ (1967) Directional change in flying locusts. J Insect Physiol 13: 1055–1063
Eaton CR (1984) Neural mechanisms of startle behavior. PlenumPress, New York
Fraser P (1977) Cereal ablation modifies tethered behavior of cockroach. Nature 268: 523–524
Gettrup E, Wilson DM (1964) The lift control reaction of flying locusts. J Exp Biol 41: 183–190
Gewecke M, Phillipen J (1978) Control of the horizontal flight course by air-current sense organs in Locusta migratoria. Physiol Entomol 3: 43–52
Griffin DR (1958) Listening in the dark. Yale University Press, New Haven, CT
Guthrie DM, Tindal AR (1968) The Biology of the cockroach. Edward Arnold Ltd, London
Heinzel H-G (1983) Rezeption von Luftströmungen und ihre Bedeutung für den Flug der Wanderheuschrecke. Biona Rep 2. Akad Wiss Lit Mainz. G. Fischer, Stuttgart
Jensen M (1956) Biology and physics of locust flight. III. The aerodynamics of locust flight. Phil Trans R Soc Lond 239: 511–552
Jones G, Rayner JMV (1988) Flight performance, foraging tactics and echolocation in free-living Daubenton's bats, Myotis daubentoni (Chiroptera: Vespertilionidae). J Zool 215: 113–132
Kolton L, Camhi JM (1993) Re-evaluating the directional sensitivity of identified giant interneurons of the cockroach. Soc Neurosci Abstr 19: 70.2
Kutsch W (1969) Neromuskuläre Aktivität bei verschiedenen Verhaltensweisen von drei Grillenarten. Z Vergl Physiol 63: 335–378
Libersat F (1992) Modulation of flight by the giant interneurons of the cockroach. J Comp Physiol A 170: 379–392
Libersat F, Hoy RR (1991) Ultrasonic startle behavior in bushcrickets (Orthoptera; Tettigoniidae). J Comp Physiol A 169: 507–514
Libersat F, Levy A, Camhi JM (1989) Multiple feedback loops in the flying cockroach: Excitation of the dorsal and inhibition of the ventral giant interneurons. J Comp Physiol A 165: 651–668
Liebenthal E, Uhlmann O, Camhi JM (1994) Critical parameters of the spike trains in a cell assembly: coding of turn direction by the giant interneurons of the cockroach. J Comp Physiol A 174: 281–296
May ML, Hoy RR (1990a) Ultrasound-induced yaw movements in the flying Australian field cricket (Teleogryllus oceanicus). J Exp Biol 149: 177–189
May ML, Hoy RR (1990b) Leg-induced steering in flying crickets. J Exp Biol 151: 485–488
Merzkirch CH (1974) Flow visualization. Academic Press, New York
Miller LA (1975) The behavior of flying green lacewings, Chrysopa carnea, in the presence of ultrasound. J Insect Physiol 21: 205–219
Miller LA, Olesen J (1979) Avoidance behavior in green lacewings. I. Behavior of free flying green lacewings to hunting bats and ultrasound. J Comp Physiol 131: 113–120
Moiseff A, Pollack GS, Hoy RR (1978) Steering responses of flying crickets to sound and ultrasound: Mate attraction and predator avoidance. Proc Natl Acad Sci USA 75: 4052–4056
Nachtigall W (1989) Mechanics and aerodynamics of flight. In: Goldsworthy GJ, Wheeler CH (eds) Insect Flight. CRC Press, Boca Raton, FL, pp 1–29
Nolen TG, Hoy RR (1986) Phonotaxis of flying crickets. I. Attraction to the calling song and avoidance of bat-like ultrasound are discrete behaviors. J Comp Physiol A 159: 423–439
Nye W, Ritzmann RE (1992) Motion analysis of leg joints associated with escape turns of the cockroach, Periplaneta americana. J Comp Physiol A 171: 183–194
Ramirez JM, Pearson KG (1988) Flight in motoneurons supplying bifunctional muscles in locusts. J Neurobiol 19: 257–282
Ritzmann RE (1993) The neural organization of cockroach escape and its role in context dependent orientation. In: Beer RD, Ritzmann RE, McKenna T (eds) Biological neural networks in invertebrate neuroethology and robotics. Academic Press, New York, pp 113–137
Robert D (1989) The auditory behavior of flying locusts. J Exp Biol 147: 279–301
Robert D, Rowell CHF (1992) Locust flight steering: Head movements and the organization of corrective maneuvers. J Comp Physiol A 171: 41–51
Roeder KD (1948) Organization of the ascending giant fiber system of the cockroach Periplaneta americana. J Exp Zool 108: 243–261
Roeder KD (1962) The behavior of free flying moths in the presence of artificial ultrasonic pulses. Anim Behav 10: 300–304
Roth LM, Willis ER (1960) Biotic associations of cockroaches. Smithson Mise Colins 141: 1–470
Rowell CHF (1993) Intersegmental coordination of flight steering in locusts. Sem Neurosci 5: 59–66
Schnitzler HU (1987) Echoes of fluttering insects: Information for echolocating bats. In: Fenton MB, Racey P, Rayner JMV (eds) Recent advances in the study of bats. Cambridge Univ Press, Cambridge, pp 229–243
Shaw SR (1990) A missing link in insect audition. Soc Neurosci Abstr 16: 400
Taylor CP (1981) Contribution of compound eyes and ocelli to steering of locusts in flight. J Exp Biol 93: 1–32
Thüring DA (1986) Variability of motor output during flight steering in locusts. J Comp Physiol A 158: 653–664
Walker EP (1964) Mammals of the world, Vol 1. The Johns Hopkins Press, Baltimore MD
Webster FA, Griffin DR (1962) The role of flight membranes in insect capture by bats. Anim Behav 10: 332–340
Westin J, Langberg J, Camhi JM (1977) Responses of giant interneurons of the cockroach Periplaneta americana to wind puffs of different directions and velocities. J Comp Physiol 121: 307–324
Wilson DM (1962) Bifunctional muscles in the thorax of grasshoppers. J Exp Biol 39: 669–677
Wolf H (1990) On the function of a locust flight steering muscle and its inhibitory innervation. J Exp Biol 150: 55–80
Yager D (1993) Cockroach homolog of mantis tympanal nerve. Soc Neurosci Abstr 19: 142.12
Yager DD, May ML, Fenton B (1990) Ultrasound-triggered, flight-gated evasive maneuvers in the flying mantis, Parasphendale agrionina. J Exp Biol 152: 17–39
Zarnack W, Möhl B (1977) Activity of the direct downstroke flight muscles of Locusta migratoria (L.) during steering behavior in flight. I. Patterns of time shift. J Comp Physiol 118: 215–233
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Ganihar, D., Libersat, F., Wendler, G. et al. Wind-evoked evasive responses in flying cockroaches. J Comp Physiol A 175, 49–65 (1994). https://doi.org/10.1007/BF00217436
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DOI: https://doi.org/10.1007/BF00217436