Abstract
The planthopper insect Issus produces one of the fastest and most powerful jumps of any insect. The jump is powered by large muscles that are found in its thorax and that, in other insects, contribute to both flying and walking movements. These muscles were therefore analysed by transmission electron microscopy to determine whether they have the properties of fast-acting muscle used in flying or those of more slowly acting muscle used in walking. The muscle fibres are arranged in a parallel bundle that inserts onto an umbrella-shaped tendon. The individual fibres have a diameter of about 70 μm and are subdivided into myofibrils a few micrometres in diameter. No variation in ultrastructure was observed in various fibres taken from different parts of the muscle. The sarcomeres are about 15 μm long and the A bands about 10 μm long. The Z lines are poorly aligned within a myofibril. Mitochondrial profiles are sparse and are close to the Z lines. Each thick filament is surrounded by 10–12 thin filaments and the registration of these arrays of filaments is irregular. Synaptic boutons from the two excitatory motor neurons to the muscle fibres are characterised by accumulations of ~60 translucent 40-nm-diameter vesicle profiles per section, corresponding to an estimated 220 vesicles, within a 0.5-μm hemisphere at a presynaptic density. All ultrastructural features conform to those of slow muscle and thus suggest that the muscle is capable of slow sustained contractions in keeping with its known actions during jumping. A fast and powerful movement is thus generated by a slow muscle.




Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Abercrombie M (1946) Estimation of nuclear population from microtome sections. Anat Rec 94:239–247
Askew GN, Marsh RL (2002) Muscle designed for maximum short-term power output: quail flight muscle. J Exp Biol 205:2153–2160
Atwood HL, Lang F, Morin WA (1972) Synaptic vesicles: selective depletion in crayfish excitatory and inhibitory axons. Science 176:1353–1355
Bernstein SI, O'Donnell PT, Cripps RM (1993) Molecular genetic analysis of muscle development, structure and function in Drosophila. Int Rev Cytol 143:63–152
Biserova NM, Pflüger HJ (2004) The ultrastructure of locust pleuroaxillary “steering” muscles in comparison to other skeletal muscles. Zoology 107:229–242
Bräunig P, Burrows M (2008) Neurons controlling jumping in froghopper insects. J Comp Neurol 507:1065–1075
Burrows M (1969) The mechanics and neural control of the prey capture strike of the Mantid shrimps Squilla and Hemisquilla. Z Vergl Physiol 62:361–381
Burrows M (1973) Physiological and morphological properties of the metathoracic common inhibitory neuron of the locust. J Comp Physiol 82:59–78
Burrows M (2009) Jumping performance of planthoppers (Hemiptera, Issidae). J Exp Biol 212:2844–2855
Burrows M, Bräunig P (2010) Actions of motor neurons and leg muscles in jumping by planthopper insects (Hemiptera, Issidae). J Comp Neurol 518:1349–1369
Burrows M, Hoyle G (1972) Neuromuscular physiology of the strike mechanism of the mantis shrimp, Hemisquilla. J Exp Zool 179:395–416
Burrows M, Morris O (2003) Jumping and kicking in bush crickets. J Exp Biol 206:1035–1049
Burrows M, Shaw SR, Sutton GP (2008) Resilin and cuticle form a composite structure for energy storage in jumping by froghopper insects. BMC Biol 6:41
Cochrane DG, Elder HY, Usherwood PNR (1972) Physiology and ultrastructure of phasic and tonic skeletal muscle fibres in the locust, Schistocerca gregaria. J Cell Sci 10:419–441
Crossley AC (1978) Morphology and development of the Drosophila muscular system. In: Ashburner M, Wright TRF (eds) The genetics and biology of Drosophila, vol 2b. Academic Press, London, pp 499–560
Elder HY (1971) High frequency muscles used in sound production by a katydid. II. Ultrastructure of the singing muscles. Biol Bull 141:411–434
Elder HY (1975) Muscle structure. In: Usherwood PNR (ed) Insect muscle. Academic Press, London, pp 1–74
Ellington CP (1985) Power and efficiency of insect flight muscle. J Exp Biol 115:293–304
Hoyle G (1969) Comparative aspects of muscle. Annu Rev Physiol 31:43–84
Hoyle G (1978) Distribution of nerve and muscle fibre types in locust jumping muscle. J Exp Biol 73:205–233
Jahromi SS, Atwood HL (1968) Correlation of structure, speed of contraction and total tension in fast and slow abdominal muscle fibres of the lobster (Homarus americanus). J Exp Zool 171:25–38
Jahromi SS, Atwood HL (1969) Structural features of muscle fibres in the cockroach leg. J Insect Physiol 15:2255–2262
Josephson RK (1993) Contraction dynamics and power output of skeletal muscle. Annu Rev Physiol 55:527–546
Josephson RK, Elder HY (1968) Rapidly contracting muscles used in sound production by a katydid. Biol Bull 135:409
McNeill P, Burrows M, Hoyle G (1972) Fine structure of muscles controlling the strike of the Mantis shrimp, Hemisquilla. J Exp Zool 179:395–416
Pringle JWS (1975) Insect flight. Oxford University Press, Oxford
Pringle JWS (1981) The evolution of fibrillar muscle in insects. J Exp Biol 94:1–14
Reger JF, Cooper DP (1967) A comparative study of the fine structure of the basalar muscle of the wing and tibial extensor muscle of the leg of the lepidopteran Achalarus lyciades. J Cell Biol 33:531–542
Rosenbluth J (1969) Sarcoplasmic reticulum of an unusually fast-acting crustacean muscle. J Cell Biol 42:534–547
Smith DS (1965) The organization of flight muscle in an aphid, Megoura viciae (Homoptera). With a discussion on the structure of synchronous and asynchronous striated muscle fibres. J Cell Biol 27:379–393
Titmus MJ (1981) Ultrastructure of identified fast excitatory, slow excitatory and inhibitory neuromuscular junctions in the locust. J Neurocytol 10:363–385
Tregear RT (1977) Insect flight muscle. Proceedings of the Oxford symposium. North-Holland, Amsterdam
Weis-Fogh T (1956) Tetanic force and shortening in locust flight muscle. J Exp Biol 33:668–684
Weis-Fogh T, Alexander RM (1977) The sustained power output from striated muscle. In: Pedley TJ (ed) Scale effects in animal locomotion. Academic Press, London, pp 511–525
Wilson DM (1962) Bifunctional muscles in the thorax of grasshoppers. J Exp Biol 39:669–677
Acknowledgements
We thank Christine Böhme for help in embedding the tissue, Zhiyuan Lu and Jola Borycz for assistance in preparing and cutting the sections and Dorota Tarnogarska for helping M.B. with the electron microscope.
Author information
Authors and Affiliations
Corresponding author
Additional information
The experimental work at Dalhousie University was supported by NSERC Discovery grant DIS 0000065 (to I.A.M.). The work at Cambridge and Aachen received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.
Rights and permissions
About this article
Cite this article
Burrows, M., Meinertzhagen, I.A. & Bräunig, P. Slowly contracting muscles power the rapid jumping of planthopper insects (Hemiptera, Issidae). Cell Tissue Res 355, 213–222 (2014). https://doi.org/10.1007/s00441-013-1731-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00441-013-1731-6


