Neuromuscular Mechanisms of Insect Flight

  • Ann E. Kammer
  • Mary B. Rheuben


The stringent requirements for successful flapping flight have resulted in remarkable adaptions of the skeleton, muscles and nervous system of animals capable of this means of locomotion. The wings have a large surface area but are lightweight to reduce the inertial costs of flapping. The flight muscles can contract and relax repeatedly and rapidly. Their high metabolic rate is adequately supported by sufficient fuel and oxygen that in many species flights lasting for hours are possible. The central nervous system produces the motor output that coordinates the contractions of the flight muscles and integrates information from a variety of receptors to adjust the motor pattern as required by environmental stimuli and the behavior of the insect. Some of these aspects of insect flight are discussed in other chapters of this volume. In this chapter we consider three topics: (1) flight muscles and their innervation, (2) motor patterns and their possible usefulness as an indicator of metabolic costs, and (3) putative roles of octopamine in flight.


Motor Unit Motor Pattern Flight Muscle Indirect Flight Muscle Insect Flight 
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  1. Altman, J.S. and Tyrer, N.M. 1977. The locust wing hinge stretch receptors. I. Primary sensory neurones with enormous central arborizations. J. Comp. Neurol. 172, 409–430.Google Scholar
  2. Bartholomew, B.A. and Casey, T.M. 1978. Oxygen consumption of moths during rest, pre-flight warm-up, and flight in relation to body size and wing morphology. J. Exp. Biol. 76, 11–25.Google Scholar
  3. Bastian, J. 1972. Neuro-muscular mechanisms controlling a flight maneuver in the honey bee. J. Comp. Physiol. 77, 126–140.CrossRefGoogle Scholar
  4. Bastian, J. and Esch, H. 1970. The nervous control of the indirect flight muscles of the honey bee. Z. Vergl. Physiol. 67, 307–324.Google Scholar
  5. Bentley, D.R. 1973. “Postembryonic development of insect motor systems,” in: Developmental Neurobiology of Arthropods, (D. Young, ed.), Cambridge University Press (147–177).Google Scholar
  6. Bodnaryk, R.P. 1979. Identification of specific dopamine-and octopamine-sensitive adenylate cyclases in the brain of Mamestra configurata Wlk. Insect Biochem. 9, 155–162.CrossRefGoogle Scholar
  7. Bodnaryk, R.P. 1980. Changes in brain octopamine levels during metamorphosis of the moth Mamestra configurata Wlk. Insect Biochem. 10, 169–173.CrossRefGoogle Scholar
  8. Burns, M.D. and Usherwood, P.N.R. 1979. The control of walking in Orthoptera. H. Motor neurone activity in nornel free-walking animals. J. Exp. Biol. 79, 69–98.Google Scholar
  9. Candy, D.J. 1978. The regulation of locust flight muscle metabolism by octopamine and other compounds. insect Biochem. 8, 177–182.Google Scholar
  10. Casaday, G.B. and Camhi, J.M. 1976. Metamorphosis of flight motor neurons in the moth Manduca sexta. J. Comp. Physiol. 112, 143–158.CrossRefGoogle Scholar
  11. Casey, T.M. 1976. Flight energetics of sphinx moths: power input during hovering flight. J. Exp. Biol. 64, 529–543.PubMedGoogle Scholar
  12. Casey, T.M. 1980. Flight energetics and heat exchange of gypsy moths in relation to air temperature. J. Exp. Biol. 88, 133–145.Google Scholar
  13. Casey, T.M. 1981. Energetics and thermoregulation of Malacosoma americanum (Lepidoptera: Lasiocampidae) during hovering flight. J. Comp. Physiol. (In press).Google Scholar
  14. Clark, H.W. 1940. The adult musculature of the anisopterous dragonfly thorax. J. Morph. 67, 523–565.CrossRefGoogle Scholar
  15. Clark, R. 1976. Structural and functional changes in an identified cricket neuron after separation from the soma. I. Structural changes. J. Comp. Neurol. 170, 253–266.Google Scholar
  16. Coggshall, J.C. 1978. Neurons associated with the dorsal longitudinal flight muscles of Drosophila melanogaster. J. Comp. Neurol. 177, 707–720.PubMedCrossRefGoogle Scholar
  17. Davis, N.T. 1977. Motor neurons of the indirect flight muscles of Dysdercus fulvoniger. Ann. Ent. Soc. Am. 70, 377–386.Google Scholar
  18. Davis, N.T. and Alanis, J. 1979. Morphological and electrophysiological characteristics of a dorsal unpaired median neuron of the cricket, Acheta domesticus. Comp. Biochem. Physiol. 62A, 777–788.Google Scholar
  19. Delcomyn, F. and Usherwood, P.N.R. 1973. Motor activity during walking in the cockroach Periplaneta americana. I. Free walking. J. Exp. Biol. 59, 629–642.Google Scholar
  20. Downer, R.G.H. 1979a. Trehalose production in isolated fat body of the American cockroach, Periplaneta americana. Comp. Biochem. Physiol. 62C, 31–34.Google Scholar
  21. Downer, R.G.H. 1979b. Induction of hypertrehalosemia by excitation in Periplaneta americana. J. Insect Physiol. 25, 59–63.CrossRefGoogle Scholar
  22. Downer, R.G.H. 1980. “Short-term hypertrehalosemia induced by octopamine in the american cockroach, Periplaneta americana L.,” in: Insect Neurobiology and Pesticide Action, (Neurotox 79), London: Soc. Chem. Industry (335–339).Google Scholar
  23. Dymond, G.R. and Evans, P.D. 1979. Biogenic amines in the nervous system of the cockroach, Periplaneta americana: association of octopamine with mushroom bodies and dorsal unpaired median (DUM) neurones. Insect Biochem. 9, 535–545.CrossRefGoogle Scholar
  24. Elder, H.Y. 1975. “Muscle structure,” in: Insect Muscle (P.N.R. Usherwood, ed.), Academic Press, New York (1–74).Google Scholar
  25. Esch, H. 1964. Über den Zusammenhang zwischen Temperatur, Aktionspotentialen und Thoraxbewegungen bei der Honigbiene (Apis mellifica L.). Z. Vergl. Physiol. 48, 547–551.Google Scholar
  26. Esch, H. and Bastian, J. 1968. Mechanical and electrical activity in the indirect flight muscles of the honey bee. Z. Vergl. Physiol. 58, 429–440.Google Scholar
  27. Esch, H., Nachtigall, W. and Kogge, S.M. 1975. Correlations between aerodynamic output, electrical activity in the indirect flight muscles and wing positions of bees flying in a servomechanically controlled wind tunnel. J. Comp. Physiol. 100, 147–159.CrossRefGoogle Scholar
  28. Evans, P.D. 1978. Octopamine distribution in the insect nervous system. J. Neurochem. 30, 1009–1013.CrossRefGoogle Scholar
  29. Evans, P.D. 1980. Biogenic amines in the insect nervous systems. Adv. Insect Physiol. 15, 317–473.CrossRefGoogle Scholar
  30. Evans, P.D. and Gee, J.D. 1980. Action of formamidine pesticides on octopamine receptors. Nature, Lond. 287, 60–62.CrossRefGoogle Scholar
  31. Evans, P.D. and O’Shea, M. 1978. The identification of an octopaminergic neurone and the modulation of a myogenic rhythm in the locust. J. Exp. Biol. 73, 235–260.PubMedGoogle Scholar
  32. Ewing, A.W. 1979. The role of feedback during singing and flight in Drosophila melanogaster. Physiol. Ent. 4, 329–337.Google Scholar
  33. Goosey, M.W. and Candy, D.J. 1980. The D-octopamine content of the haemolymph of the locust, Schistocerca americana gregaria and its elevation during flight. Insect Biochem. 10, 393–397.CrossRefGoogle Scholar
  34. Grillner, S. 1977. “On the neural control of movement - a comparison of different basic rhythmic behaviors,” in: Function and Formation of Neural Systems, (G.S. Stent, ed.), Dahlem Konferenzen, Berlin (197–224).Google Scholar
  35. Hanegan, J.L. and Heath, J.E. 1970. Temperature dependence of the neural control of the moth flight system. J. Exp. Biol. 53, 629–639.PubMedGoogle Scholar
  36. Harcombe, E.S. and Wyman, R.S. 1978. The cyclically repetitive firing sequences of identified Drosophila flight motoneurons. J. Comp. Physiol. 123, 271–279.CrossRefGoogle Scholar
  37. Harris-Warrick, R., Livingstone, M. and Kravitz, E. 1980. Central effects of octopamine and serotonin on postural motor systems in the lobster. Soc. Neurosci. Abs. 6, 27.Google Scholar
  38. Heide, G. 1979. Proprioceptive feedback dominates the central oscillator in the patterning of the flight motoneuron output in Tipula (Diptera). J. Comp. Physiol. A134, 177–189.CrossRefGoogle Scholar
  39. Heinertz, R. 1976. Untersuchungen am thorakalen Nervensystem von Antheraea polyphemus Cr. (Lepidoptera) unter besonderer Berücksichtigung der Metamorphose. Rev. Suisse Zool. 83, 215–242.Google Scholar
  40. Heinrich, B. 1971. Temperature regulation of the sphinx moth, Manduca sexta. I. Flight energetics and body temperature during free and tethered flight. J. Exp. Biol. 54, 141–152.Google Scholar
  41. Hinks, C.F. 1967. Relationship between serotonin and the circadian rhythm in some nocturnal moths. Nature, Lond. 214, 386–387.CrossRefGoogle Scholar
  42. Hollingworth, R.M. and Murdock, L.L. 1980. Formamidine pesticides: octopamine-like actions in a firefly. Science 208, 74–76.PubMedCrossRefGoogle Scholar
  43. Hoyle, G. 1974. A function for neurons (DUM) neurosecretory on skeletal muscle of insects. J. Exp. Zool. 189, 401–406.PubMedCrossRefGoogle Scholar
  44. Hoyle, G. 1975. Evidence that insect dorsal unpaired median (DUM) neurons are octopaminergic. J. Exp. Zool. 193, 425–431.PubMedCrossRefGoogle Scholar
  45. Hoyle, G. 1978. The dorsal, unpaired, median neurons of the locust metathoracic ganglion. J. Neurobiol. 9, 43–57.PubMedCrossRefGoogle Scholar
  46. Hoyle, G. and Barker, D.L. 1975. Synthesis of octopamine by insect dorsal median unpaired neurons. J. Exp. Zool. 193, 433–439.PubMedCrossRefGoogle Scholar
  47. Hoyle, G., Colquhoun, W. and Williams, M. 1980. Fine structure of an octopaminergic neuron and its terminals. J. Neurobiol. 11, 103–126.PubMedCrossRefGoogle Scholar
  48. Ikeda, K. and Boettiger, E.G. 1965. Studies on the flight mechanism of insects. U. The innervation and electrical activity of the fibrillar muscles of the bumblebee, Bombus. J. Insect Physiol. 11, 779–789.Google Scholar
  49. Josephson, R.K. 1975. Extensive and intensive factors determining the performance of striated muscle. J. Exp. Zool. 194, 135–153.Google Scholar
  50. Josephson, R.K. 1981. “Temperature and the mechanical performance of insect muscle,” in: Insect Thermoregulation, (B. Heinrich, ed.), John Wiley & Sons, New York (19–44).Google Scholar
  51. Kammer, Ann E. 1967. Muscle activity during flight in some large Lepidoptera. J. Exp. Biol. 47, 277–295.PubMedGoogle Scholar
  52. Kammer, A.E. 1968. Motor patterns during flight and warm-up in Lepidoptera. J. Exp. Biol. 48, 89–109.Google Scholar
  53. Kammer, A.E. 1970. A comparative study of motor patterns during pre-flight warm-up in hawkmoths. Z. Vergl. Physiol. 70, 4556.Google Scholar
  54. Kammer, A.E. 1971. The motor output during turning flight in a hawkmoth, Manduca sexta. J. Insect Physiol. 17, 1073–1086.CrossRefGoogle Scholar
  55. Kammer, A.E. and Heinrich, B. 1974. Metabolic rates related to muscle activity in bumblebees. J. Exp. Biol. 61, 219–227.PubMedGoogle Scholar
  56. Kammer, A.E. and Heinrich, B. 1978. Insect flight metabolism. Adv. Insect Physiol. 13, 133–228.CrossRefGoogle Scholar
  57. Kammer, A.E. and Kinnamon, S.C. 1979. Maturation of the flight motor pattern without movement in Manduca sexta. J. Comp. Physiol. 130, 29–37.CrossRefGoogle Scholar
  58. Kelsey, L.P. 1957. The skeleto-motor mechanism of the dobson fly, Corydalus cornutus. Part II. Pterothorax. Cornell Univ. Agric. Exp. Stat., Ithaca, N.Y., Memoir 346.Google Scholar
  59. Neville, A.D. and Weis-Fogh, T. 1963. The effect of temperature on locust flight muscle. J. Exp. Biol. 40, 111–121.Google Scholar
  60. Kinnamon, S.C., Klaassen, L.W. and Kammer, A.E. 1980. Habituation and effects of an octopamine agonis in the developing moth flight control system. Soc. Neurosci. Abs. 6, 627.Google Scholar
  61. Klaassen, L.W. and Kammer, A.E. 1980. Modulation of neuromuscular transmission by octopamine in developing and adult moths (Man-duca sexta). Soc. Neurosci. Abs. 6, 627.Google Scholar
  62. Kutsch, W. and Usherwood, P.N.R. 1970. Studies of the innervation and electrical activity of flight muscles in the locust, Schistocerca gregaria. J. Exp. Biol. 52, 299–312.Google Scholar
  63. Livingstone, M.S., Harris-Warrick, R.M. and Kravitz, E.A. 1980. Serotonin and octopamine produce opposite postures in lobsters. Science 208, 76–79.PubMedCrossRefGoogle Scholar
  64. Maxwell, G.D., Tait, J.F. and Hildebrand, J.G. 1978. Regional synthesis of neurotransmitter candidates in the CNS of the moth Manduca sexta. Comp. Biochem. Physiol. 61C, 109–119.Google Scholar
  65. Muszynska-Pytel, M. and Cymborowski, B. 1978. The role of serotonin in regulation of the circadian rhythms of locomotor activity in the cricket (Acheta domesticus L.). I. Circadian variations in serotonin concentration in the brain and hemolymph. Comp. Biochem. Physiol, 59C, 13–15.Google Scholar
  66. Nachtigall, W. and Wilson, D.M. 1967. Neuro-muscular control of dipteran flight. J. Exp. Biol. 47, 77–97.PubMedGoogle Scholar
  67. Nathanson, J.A. and Greengard, P. 1973. Octopamine-sensitive adenylate cyclase: evidence of a biological role of octopamine in nervous tissue. Science 108, 308–310.CrossRefGoogle Scholar
  68. Olesen, J. and Miller, L.A. 1979. Avoidance behavior in green lacewings. H. Flight muscle activity. J. Comp. Physiol. 131, 121–128.Google Scholar
  69. Osborne, M.P. 1975. “The ultrastructure of nerve-muscle synapses,” in: Insect Muscle, (P.N.R. Usherwood, Ed.), Academic Press, New York (151–205).Google Scholar
  70. O’Shea, M. and Evans, P.D. 1979. Potentiation of neuromuscular transmission by an octopaminergic neurone in the locust. J. Exp. Biol. 79, 169–190.Google Scholar
  71. Pearson, K.G. and Iles, J.F. 1970. Discharge patterns of coxal levator and depressor motoneurons of the cockroach Periplaneta americana. J. Exp. Biol. 52, 139–165.PubMedGoogle Scholar
  72. Piek, T. and Njio, K.D. 1979. Morphology and electrochemistry of insect muscle fibre membrane. Adv. Insect Physiol. 14, 185250.Google Scholar
  73. Plotnikova, S.I. 1969. Effector neurons with several axons in the ventral nerve cord of the Asia grasshopper Locusta migratoria. J. Evol. Biochem. Physiol. 5, 276–277 (English trans.).Google Scholar
  74. Pringle, J.W.S. 1949. The excitation and contraction of the flight muscles of insects. J. Physiol. 108, 226–232.Google Scholar
  75. Pringle, J.W.S. 1957. Insect Flight. Cambridge University Press. 132 pp.Google Scholar
  76. Pringle, J.W.S. 1978. Stretch activation of muscle: function and mechanism. Proc. Roy. Soc. Lond. B 201, 107–130.CrossRefGoogle Scholar
  77. Rees, D. and Usherwood, P.N.R. 1972. Fine structure of normal and degenerating motor axons and nerve-muscle synapses in the locust, Schistocerca 9regaria. Comp. Biochem. Physiol. 43, 83–101.Google Scholar
  78. Robertson, H.A. and Steele, J.E. 1972. Activation of insect nerve cord phosphorylase by octopamine and adenosine 3’, 5’-monophosphate. J. Neurochem. 19, 1603–1606.PubMedCrossRefGoogle Scholar
  79. Robertson, H.A. and Steele, J.E. 1973. Effect of monophenolic amines on glycogen metabolism in the nerve-cord of the American cockroach, Periplaneta americana. Insect Biochem. 3, 53–59.CrossRefGoogle Scholar
  80. Robertson, H.A. and Steele, J.E. 1974. Octopamine in the insect central nervous system: distribution, biosynthesis and possible physiological role. J. Physiol. Lond. 237, 34–35P.Google Scholar
  81. Roeder, K.D. 1951. Movements of the thorax and potential changes in the thoracic muscles of insects during flight. Biol. Bull. 100, 95–106.CrossRefGoogle Scholar
  82. Rosenbluth, J. 1973. Membrane specialization at an insect myoneural junction. J. Cell Biol. 59, 143–149.PubMedCrossRefGoogle Scholar
  83. Rheuben, M.B. 1974. The permeability of the “synaptic complex” of moth neuromuscular junctions. Physiologist 17, 388.Google Scholar
  84. Rheuben, M.B. and Kammer, A.E. 1980. Comparison of slow larval and fast adult muscle innervated by the same motor neurone. J. Exp. Biot, 84, 103–118.Google Scholar
  85. Rheuben, M.B. and Reese, T.S. 1978. Three-dimensional structure and membrane specializations of the moth excitatory neuromuscular synapse. J. Ultrastruc. Res. 65, 95–111.CrossRefGoogle Scholar
  86. Simmons, P. 1977. The neuronal control of dragonfly flight. I. Anatomy. J. Exp. Biol. 71, 123–140.Google Scholar
  87. Sotavalta, O. 1953. Recordings of high wing-stroke and thorax vibration frequency in some midges. Biol. Bull. Marine Biol. Lab. Woods Hole. 104, 439–444.CrossRefGoogle Scholar
  88. Steele, J.E. and Chan, F. 1980. “Na+-dependent respiration in the insect nerve cord and its control by octopamine,” in: Insect Neurobiology and Pesticide Action, (Neurotox 79), London: Soc. Chem. Industry (347–350).Google Scholar
  89. Stokes, D.R., Josephson, R.K. and Price, R.B. 1975. Structural and functional heterogeneity in an insect muscle. J. Exp. Zool. 194, 379–408.PubMedCrossRefGoogle Scholar
  90. Van Der Horst, D.J., Houben, N.M.D. and Beenakkers, A.M. Th. 1980.Google Scholar
  91. Dynamics of energy substrates in the haemolymph of Locusta migratoria during flight. J. Insect Physiol. 26, 441–448.Google Scholar
  92. Weis-Fogh, T. 1952. Fat combustion and metabolic rate of flying locusts. Phil. Trans. Roy. Soc. Lond. B237, 1–36.Google Scholar
  93. Weis-Fogh, T. 1975. “Flapping flight and power in birds and insects, conventional and novel mechanisms,” in: Swimming and Flying in Nature, Vol. II, (T.Y.-F. Wu, C.J.Brokaw and C. Brennen, eds.), Plenum, New York (729–762).Google Scholar
  94. Weis-Fogh, T. 1977. “Dimensional analysis of hovering flight,” in: Scale Effects in Animal Location, (T.S. Pedley, Ed.), Academic Press, New York (405–420).Google Scholar
  95. Wilson, D.M. 1966. Central nervous mechanisms for the generation of rhythmic behaviour in arthropods. Symp. Soc. Exp. Biol. 20, 199–228.PubMedGoogle Scholar
  96. Wilson, D.M. and Weis-Fogh, T. 1962. Patterned activity of coordinated motor units, studied in flying locusts. J. Exp. Biol. 39, 643–667.Google Scholar
  97. Wilson, D.M. and Wyman, R.J. 1963. Physically unpatterned nervous control of dipteran flight. J. Insect Physiol. 9, 859–965.CrossRefGoogle Scholar
  98. Wood, D.W. 1957. The effect of ions upon neuromuscular transmission in a herbivorous insect. J. Physiol. Lond. 138, 119–139.PubMedGoogle Scholar
  99. Wyman, R.J. 1966. Multistable firing patterns among several neurons. J. Neurophysiol. 29, 807–833.PubMedGoogle Scholar

Copyright information

© Plenum Press, New York 1981

Authors and Affiliations

  • Ann E. Kammer
    • 1
  • Mary B. Rheuben
    • 2
  1. 1.Division of BiologyKansas State UniversityManhattanUSA
  2. 2.Department of AnatomyMichigan State UniversityEast LansingUSA

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