Abstract
Flying insects rely on the integration of feedback signals from multiple sensory modalities. Thus, in addition to the visual input, mechanosensory information from antennae is crucial for stable flight in the hawkmoth Manduca sexta. However, the nature of compensatory reflexes mediated by mechanoreceptors on the antennae is unknown. In this study we describe an abdominal flexion response mediated by the antennal mechanosensory input during mechanical body rotations. Such reflexive abdominal motions lead to shifts in the animal’s center of mass, and therefore changes in flight trajectory. Moths respond with abdominal flexion both to visual and mechanical rotations, but the mechanical response depends on the presence of the mass of the flagellum. In addition, the mechanically mediated flexion response is about 200° out of phase with the visual response and adds linearly to it. Phase-shifting feedback signals in such a manner can lead to a more stable behavioral output response when the animal is faced with turbulent perturbations to the flight path.
Similar content being viewed by others
References
Arbas E (1986) Control of hindlimb posture by wind-sensitive hairs and antennae during locust flight. J Comp Physiol A 159(6):849–857
Autrum H (1958) Electrophysiological analysis of the visual systems in insects. Exp Cell Res 14(Suppl 5):426–439
Baader A (1988) Some motor neurones of the abdominal longitudinal muscles of grasshoppers and their role in steering behaviour. J Exp Biol 134:455–462
Baader A (1990) The posture of the abdomen during locust flight: regulation by steering and ventilatory interneurones. J Exp Biol 151:109–131
Budick SA, Reiser MB, Dickinson MH (2007) The role of visual and mechanosensory cues in structuring forward flight in Drosophila melanogaster. J Exp Biol 210(23):4092–4103
Burkhardt D, Schneider G (1957) Die Antennen von Calliphora als Anzeiger der Fluggeschwindigkeit. Z Naturf 12b:139–143
Burrows M (1996) The neurobiology of an insect brain. Oxford University Press, New York
Camhi J (1970a) Sensory control of abdomen posture in flying locusts. J Exp Biol 52(3):533
Camhi J (1970b) Yaw-correcting postural changes in locusts. J Exp Biol 52:519–531
Collett T, Nalbach H, Wagner H (1993) Visual stabilization in arthropods. Rev Oculomot Res 5:239–263
Dickinson M (1999) Haltere-mediated equilibrium reflexes of the fruit fly, Drosophila melanogaster. Philos Trans R Soc Lond B Biol Sci 354(1385):903–916
Dickinson MH, Lehmann FO, Sane SP (1999) Wing rotation and the aerodynamic basis of insect flight. Science 284:1954–1960
Dorf R, Bishop R (2008) Modern control systems. Prentice-Hall, Englewood Cliffs
Fox J, Daniel T (2008) A neural basis for gyroscopic force measurement in the halteres of Holorusia. J Comp Physiol A 194(10):887–897
Fox J, Fairhall A, Daniel T (2010) Encoding properties of haltere neurons enable motion feature detection in a biological gyroscope. Proc Natl Acad Sci USA 107(8):3840–3845
Frye M (2001) Encoding properties of the wing hinge stretch receptor in the hawkmoth Manduca sexta. J Exp Biol 204(Pt 21):3693–3702
Gewecke M (1970) Antennae: another wind-sensitive receptor in locusts. Nature 225(5239):1263–1264
Gewecke M, Niehaus M (1981) Flight and flight control by the antennae in the Small Tortoiseshell (Aglais urticae L., Lepidoptera). J Comp Physiol A 145(2):249–256
Gewecke M, Heinzel H, Philippen J (1974) Role of antennae of the dragonfly Orthetrum cancellatum in flight control. Nature 249:584–585
Goodman LJ (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 43:385–407
Götz K (1968) Flight control in Drosophila by visual perception of motion. Kybernetik 4(6):199–208
Hedrick T (2008) Software techniques for two- and three-dimensional kinematic measurements of biological and biomimetic systems. Bioinspir Biomim 3(3):34,001
Hedrick T, Daniel T (2006) Flight control in the hawkmoth Manduca sexta: the inverse problem of hovering. J Exp Biol 209(Pt 16):3114–3130
Hensler K (1988) The pars intercerebralis neurone PI (2) 5 of locusts: convergent processing of inputs reporting head movements and deviations from straight flight. J Exp Biol 140:511–533
Heran H (1959) Wahrnehmung und Regelung der Flugeigengeschwindigkeit bei Apis mellifica L. J Comp Physiol A 42(2):103–163
Kamikouchi A, Inagaki H, Effertz T, Hendrich O, Fiala A, Göpfert M, Ito K (2009) The neural basis of Drosophila gravity-sensing and hearing. Nature 458(7235):165–171
Kloppenburg P, Camazine SM, Sun XJ, Randolph P, Hildebrand JG (1997) Organization of the antennal motor system in the sphinx moth Manduca sexta. Cell Tissue Res 287(2):425–433
Laughlin S, Weckström M (1993) Fast and slow photoreceptors—a comparative study of the functional diversity of coding and conductances in the Diptera. J Comp Physiol A 172(5):593–609
Mountcastle AM, Daniel TL (2009) Aerodynamic and functional consequences of wing compliance. Exp Fluids 45(5):873–882
Nalbach G, Hengstenberg R (1994) The halteres of the blowfly Calliphora 2. 3-Dimensional organization of compensatory reactions to real and simulated rotations. J Comp Physiol A 175(6):695–708
Niehaus M (1981) Flight and flight control by the antennae in the Small Tortoiseshell (Aglais urticae L., Lepidoptera). J Comp Physiol A 145(2):257–264
Pringle J (1948) The gyroscopic mechanism of the halteres of Diptera. Philos Trans R Soc Lond B Biol Sci 233(602):347–384
Reichert H (1989) Neural mechanisms underlying axial/appendicular steering reactions in locust flight. Am Zool 29(1):161–169
Reiser M, Dickinson M (2008) A modular display system for insect behavioral neuroscience. J Neurosci Methods 167(2):127–139
Sane S, Dieudonne A, Willis M, Daniel T (2007) Antennal mechanosensors mediate flight control in moths. Science 315(5813):863–866
Sherman A, Dickinson M (2003) A comparison of visual and haltere-mediated equilibrium reflexes in the fruit fly Drosophila melanogaster. J Exp Biol 206(Pt 2):295–302
Sherman A, Dickinson M (2004) Summation of visual and mechanosensory feedback in Drosophila flight control. J Exp Biol 207(Pt 1):133–142
Taylor CP (1981a) Contribution of compound eyes and ocelli to steering of locusts in flight: I. Behavioural analysis. J Exp Biol 93:1–18
Taylor CP (1981b) Contribution of compound eyes and ocelli to steering of locusts in flight: II. Timing changes in flight motor units. J Exp Biol 93:19–31
Taylor G, Krapp H (2008) Sensory systems and flight stability: what do insects measure and why? Adv Insect Physiol 34:231–316
Theobald JC (2004) Perceiving motion in the dark. PhD thesis, University of Washington, Seattle, WA
Theobald JC, Warrant EJ, O’Carroll DC (2010) Wide-field motion tuning in nocturnal hawkmoths. Philos Trans R Soc Lond B Biol Sci 277(1683):853–860
Warrant EJ (1999) Seeing better at night: life style, eye design and the optimum strategy of spatial and temporal summation. Vis Res 39(9):1611–1630
Acknowledgments
We thank Michael Reiser for engineering the LED panels system and for his helpful advice when setting it up, and David Williams for help with the stepper motor controller. In addition we are grateful to K. Morgansen Hill, Z. Aldworth, A. Mountcastle, B. Medina, and other members of the Daniel lab for critical reviews of the manuscript. Support was provided by the Joan and Richard Komen Endowed Chair and grants form DARPA and ONR to TLD.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplemental movie (MOV 5004 kb)
Rights and permissions
About this article
Cite this article
Hinterwirth, A.J., Daniel, T.L. Antennae in the hawkmoth Manduca sexta (Lepidoptera, Sphingidae) mediate abdominal flexion in response to mechanical stimuli. J Comp Physiol A 196, 947–956 (2010). https://doi.org/10.1007/s00359-010-0578-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-010-0578-5