Abstract
MaleHeliothis virescens (F.) (Lepidoptera: Noctuidae) were made to fly into a uniformly white and translucent tube within a large wind tunnel while responding to sex pheromone. Different visual patterns placed within the tube greatly affected the ability of the male moths to maintain upwind progress or remain oriented to the wind while in contact with the plume. Over 89% of males attempting to fly through a blank tube, lacking visual patterns, became disoriented, the males gaining or losing altitude and repeatedly hitting the sides of the tube. Patterns of 20–40 dots placed on the sides of the tube at or slightly above plume level resulted in high levels of sustained upwind flight (47–74%) relative to patterns placed directly below (30–40%), directly above (35%), or slightly below the level of the flight path (26–44%). Optimal upwind progression in pheromone-responding males occurred when image motion could be resolved both transversely (T), orthogonally to the longitudinal axis of the body relative to the horizontal plane of the environment, and longitudinally (L), along the body axis. Even very sparse patterns (single rows of dots) could elicit high levels of sustained upwind flight (53–63%) when positioned within the tube such that the males' movements would create both L and T image motion. However, successful negotiation of the tube was also unexpectedly facilitated by patterns apparently providing no horizontal transverse component for flying males but providing longitudinal flow while centering the moth in the plume through a symmetrical left-right input (4–40%).
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Baker, T. C., and Haynes, K. F. (1987). Manoeuvres used by flying male oriental fruit moths to relocate a pheromone plume in an experimentally shifted wind-field.Physiol. Entomol. 12 263–279.
Baker, T. C., and Vickers, N. J. (1994). Behavioral reaction times of male moths to pheromone filaments and visual stimuli: Determinants of flight track shape and direction. InProceedings of the XIth International Symposium on Olfaction and Taste, Sapporo, Japan, pp. 838–841.
Baker, T. C., Willis, M. A., Haynes, K. F., and Phelan, P. L. (1985). A pulsed cloud of sex pheromone elicits upwind flight in male moths.Physiol. Entomol. 10 257–265.
Collett, T. S. (1980). Some operating rules for the optomotor system of a hoverfly during voluntary flight.J. Comp. Physiol. A 138 271–282.
Collett, T. S., and Blest, A.-D. (1966). Binocular, directionally selective neurones, possibly involved in the optomotor response of insects.Nature 212 1330–1333.
David, C. T. (1979). Height control by free-flyingDrosophila.Physiol. Entomol. 4 209–216.
David, C. T. (1982a). Compensation for height in the control of groundspeed byDrosophila in a new, “barber's pole” wind tunnel.J. Comp. Physiol. A 147 485–493.
David, C. T. (1982b). Competition between fixed and moving stripes in the control of orientation by free-flyingDrosophila.Physiol. Entomol. 7 151–156.
David, C. T. (1986). Mechanisms of directional flight in wind. In Payne, T. L., Birch, M. C., and Kennedy, C. E. J. (eds.),Mechanisms in Insect Olfaction, Clarendon Press, Oxford, pp. 49–57.
David, C. T., Kennedy, J. S., Ludlow, A. R., Perry, J. N., and Wall, C. (1982). A reappraisal of insect flight towards a distant point source of wind-borne odor.J. Chem. Ecol. 8 1207–1215.
Eckert, H. (1982). The vertical-horizontal neurone (VH) in the lobula plate of the blowfly,Phaenicia.J. Comp. Physiol. A 149 195–205.
Egelhaaf, M., and Borst, A. (1993). Motion computation and visual orientation in flies.Comp. Biochem. Physiol. 104A 659–673.
Farkas, S. R., and Shorey, H. H. (1972). Chemical trail following by flying insects: A mechanism for orientation to a distant odor source.Science 178 67–68.
Fletcher, W. A., Goodman, L. J., Guy, R. G., and Mobbs, P. G. (1984). Horizontal and vertical motion detectors in the ventral nerve cord of the honeybee,Apis mellifera. J. Physiol. 351: 15P.
Gillett, J. D. (1979). Out for blood: Flight orientation up-wind in the absence of any visual cues.Mosq. News 39 221–229.
Goetz, K. G. (1972). Principles of optomotor reactions in insects.Bibl. Opthalmol. 82 252–259.
Goetz, K. G. (1975). The optomotor equilibrium of theDrosophila navigation system.J. Comp. Physiol. 99 187–210.
Gronenberg, W., and Strausfeld, N. J. (1991). Descending pathways connecting the male-specific visual system of flies to the neck and flight motor.J. Comp. Physiol. A 169: 413–426.
Hausen, K. (1982a). Motion sensitive interneurons in the optomotor system of the fly. I. The horizontal cells: Structure and function.Biol. Cybern. 45 143–156.
Hausen, K. (1982b). Motion sensitive interneurons in the optomotor system of the fly. II. The horizontal cells: Receptive field organization and response characteristics.Biol. Cybern. 46 67–79.
Ibbotson, M. R., and Goodman, L. J. (1990). Response characteristics of four wide-field motion-sensitive descending interneurons inApis mellifera.J. Exp. Biol. 148 255–279.
Ibbotson, M. R., Maddess, T., and DuBois, R. (1991). A system of insect neurons sensitive to horizontal and vertical image motion connects the medulla and midbrain.J. Comp. Physiol. A 169 355–367.
Kellogg, F. E., Frizel, D. E., and Wright, R. H. (1962). The olfactory guidance of flying insects. IV. Drosophila.Can. Entomol. 8 884–888.
Kennedy, J. S. (1940). The visual responses of flying mosquitoes.Proc. Zool. Soc. London A109 221–242.
Kennedy, J. S. (1986). Some current issues in orientation to odour sources. In Payne, T. L., Birch, M. C., and Kennedy, C. E. J. (eds.),Mechanisms in Insect Olfaction, Clarendon Press, Oxford, pp. 11–25.
Kennedy, J. S., and Marsh, D. (1974). Pheromone regulated anemotaxis in flying moths.Science 184 999–1001.
Kennedy, J. S., Ludlow, A. R., and Sanders, C. J. (1981). Guidance of flying male moths by wind-borne sex pheromone.Physiol. Entomol. 6 395–412.
Kirchner, W. H., and Srinivasan, M. V. (1989). Freely flying honeybees use image motion to estimate object distance.Naturwissenschaften 76 281–282.
Kuenen, L. P. S., and Baker, T. C. (1982). The effects of pheromone concentration on the flight behaviour of the oriental fruit moth,Grapholitha molesta.Physiol. Entomol. 7 423–434.
Ludlow, A. R. (1984).Application of Computer Modelling to Behavioural Co-ordination, Ph.D. thesis, University of London, London.
Marsh, D., Kennedy, J. S., and Ludlow, A. R. (1978). An analysis of anemotactic zigzagging flight in male moths stimulated by pheromone.Physiol. Entomol. 3 221–240.
Milde, J. J. (1993). Tangential medulla neurons in the mothManduca sexta. Structure and responses to optomotor stimuli.J. Comp. Physiol. A 173: 783–799.
Miller, J. R., and Roelofs, W. L. (1978). Sustained-flight tunnel for measuring insect responses to wind-borne sex pheromones.J. Chem. Ecol. 4 187–198.
Olberg, R. M., and Willis, M. A. (1990). Pheromone-modulated optomotor response in male gypsy moths,Lymantria dispar L.: Directionally selective visual interneurons in the ventral nerve cord.J. Comp. Physiol. A 167: 707–714.
Preiss, R. (1991). Separation of translation and rotation by means of eye-region specialization in flying gypsy moths (Lepidoptera: Lymantriidae).J. Insect Behav. 4 209–219.
Preiss, R., and Futschek, L. (1985). Flight stabilization by pheromone-enhanced optomotor responses.Naturwissenschaften 72 435–436.
Preiss, R., and Kramer, E. (1983). Stabilization of altitude and speed in tethered flying gypsy moth males: Influence of (+) and (-)-disparlure.Physiol. Entomol. 8 55–68.
Shorey, H. H., and Hale, R. L. (1965). Mass-rearing of the larvae of nine noctuid species on a simple artificial medium.J. Econ. Entomol. 58 522–524.
Steel, R. G. D., and Torrie, J. H. (1960).Principles and Procedures of Statistics, McGraw-Hill, New York, pp. 366–373.
Teal, P. E. A., Tumlinson, J. H., and Heath, R. R. (1986). Chemical and behavioral analysis of volatile sex pheromone components released by callingHeliothis virescens (F.) females (Lepidoptera: Noctuidae).J. Chem. Ecol. 12 107–126.
Vetter, R. S., and Baker, T. C. (1983). Behavioral responses of maleHeliothis virescens in a sustained-flight tunnel to combinations of seven compounds identified from female sex pheromone glands.J. Chem. Ecol. 9 947–959.
Willis, M. A., and Baker, T. C. (1984). Effects of intermittent and continuous pheromone stimulation on the flight behaviour of the oriental fruit moth,Grapholita molesta.Physiol. Entomol. 9 341–358.
Willis, M. A., and Cardé, R. T. (1990). Pheromone-modulated optomotor response in male gypsy moths,Lymantria dispar L.: Upwind flight in a pheromone plume in different wind velocities.J. Comp. Physiol. A 167: 699–706.
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Vickers, N.J., Baker, T.C. Visual feedback in the control of pheromone-mediated flight ofHeliothis virescens males (Lepidoptera: Noctuidae). J Insect Behav 7, 605–632 (1994). https://doi.org/10.1007/BF01997435
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DOI: https://doi.org/10.1007/BF01997435