Skip to main content
SpringerLink
Log in

Power and control muscles of cicada song: structural and contractile heterogeneity

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Sound production in cicadas is powered by a pair of large muscles whose contractions cause buckling of cuticular tymbals and thereby create sound pulses. Sound is modulated by control muscles that alter the stiffness of the tymbals or change the shape of the abdominal resonance chamber. Muscle ultrastructure and contractile properties were characterized for the tymbal muscle and two control muscles, the ventral longitudinal muscle and the tymbal tensor, of the periodical cicada Magicicada septendecim. The tymbal muscle is a fast muscle that is innervated by a single motoraxon. The control muscles are an order of magnitude less massive than the tymbal muscles, but their innervation patterns were considerably more complex. The tensor muscle is innervated by two axons, each of which evokes rather slow twitches, and the ventral muscle is innervated by at least six axons, some of which produce fast and the others slow contractions. Muscle contraction kinetics correlated well with ultrastructure. Fibers of the tymbal muscle and the portions of the ventral muscle thought to be fast were richly supplied with transverse tubules (T-tubules) and sarcoplasmic reticulum (SR); slow portions of the ventral muscle and the tensor muscle had relatively little SR.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3A,B
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

SR:

sarcoplasmic reticulum

TTS:

transverse tubular system

VLM:

ventral longitudinal muscle

References

  • Alexander RD (1957) Sound production and associated behavior in insects. Ohio J Sci 57:101–113

    Google Scholar 

  • Alexander RD, Moore TE (1958) Studies on the acoustical behavior of seventeen-year cicadas. Ohio J Sci 58:107–127

    Google Scholar 

  • Bennet-Clark HC (1997) Tymbal mechanics and the control of song frequency in the cicada Cyclochila australasiae. J Exp Biol 200:181-1694

    Google Scholar 

  • Dickinson MH, Tu MS (1997) The function of dipteran flight muscle. Comp Biochem Physiol 226A:223–228

    Article  Google Scholar 

  • Fonseca PJ (1991) Characteristics of the acoustic signals in nine species of cicadas (Homoptera, Cicadidae). Bioacoustics 3:173–182

    Google Scholar 

  • Fonseca PJ (1996) Sound production in cicadas: timbal muscle activity during calling song and protest song. Bioacoustics 7:13–31

    Google Scholar 

  • Fonseca PJ, Bennet-Clark HC (1998) Asymmetry of tymbal action and structure in a cicada: a possible role in the production of complex songs. J Exp Biol 201:717–730

    PubMed  Google Scholar 

  • Fonseca PJ, Hennig RM (1996) Phasic action of the tensor muscle modulates the calling song in cicadas. J Exp Biol 199:1535–1544

    PubMed  Google Scholar 

  • Fonseca PJ, Popov AV (1994) Sound radiation in a cicada: the role of different structures. J Comp Physiol 175:349–361

    Google Scholar 

  • Freere RH, Weibel ER (1967) Stereologic techniques in microscopy. J R Microsc Soc 87:25–34

    PubMed  Google Scholar 

  • Fry JC (1993) Biological data analysis. Oxford University Press, Oxford

  • Hagiwara S (1955) Neuro-muscular mechanism of sound production in the cicada. Physiol Comp Oecol 4:142–153

    Google Scholar 

  • Hagiwara S, Watanabe A (1954) Acton potentials of insect muscles examined with intracellular electrode. J Physiol (Lond) 4:65–78

    Google Scholar 

  • Hennig RM, Weber T, Moore TE, Huber F, Kleindienst H-U, Popov AV (1994) Function of the tensor muscle in the cicada Tibicen linnei. J Exp Biol 187:33–44

    PubMed  Google Scholar 

  • Josephson RK (1975) Extensive and intensive factors determining the performance of striated muscle. J Exp Biol 59:781–801

    Google Scholar 

  • Josephson RK, Young D (1981) Synchronous and asynchronous muscles in cicadas. J Exp Biol 91:219–237

    Google Scholar 

  • Josephson RK, Young D (1985) A synchronous insect muscle with an operating frequency greater than 500 Hz. J Exp Biol 118:185–208

    Google Scholar 

  • Josephson RK, Young D (1987) Fiber ultrastructure and contraction kinetics in insect fast muscles. Am Zool 27:991–1000

    Google Scholar 

  • Marlatt CL (1907) The periodical cicada. US Dept Agric Bureau Entomol Bull 71

  • Moore TE, Sawyer RT (1966) The mechanism of cicada tymbal action (Insecta: Homoptera: Cicadidae). Am Zool 6:509

    Google Scholar 

  • Myers JG (1928) The morphology of the Cicadidae (Homoptera). Proc Zool Soc London 365–472

  • Myers JG (1929) Insect singers: a natural history of the cicadas. Routledge, London

    Google Scholar 

  • Popov AV (1981) Sound production and hearing in the cicada, Cicadetta sinuatipennis Osh (Homoptera, Cicadidae). J Comp Physiol 142:271–280

    Google Scholar 

  • Pringle JWS (1954a) The mechanism of the myogenic rhythm of certain insect striated muscles. J Physiol (Lond) 124:269–291

    Google Scholar 

  • Pringle JWS (1954b) A physiological analysis of cicada song. J Exp Biol 31:525–560

    Google Scholar 

  • Pringle JWS (1957) The structure and evolution of the organs of sound production in cicadas. Proc Linn Soc London 167:144–159

    Google Scholar 

  • Reid KH (1971) Periodical cicada: mechanism of sound production. Science 172:949–951

    Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J Cell Biol 17:208–211

    CAS  Google Scholar 

  • Richardson KC, Jarett L, Finke EH (1960) Embedding epoxy resins for ultra-thin sectioning in electron microscopy. Stain Technol 35:313–323

    CAS  Google Scholar 

  • Simmons PJ (1977) Neuronal generation of singing in a cicada. Nature 270:243–245

    CAS  PubMed  Google Scholar 

  • Simmons PJ, Young D (1978) The tymbal mechanism and song patterns of the bladder cicada, Cystosoma saundersii. J Exp Biol 76:27–45

    Google Scholar 

  • Stokes DR, Josephson RK, Price RB (1975) Structural and functional heterogeneity in an insect muscle. J Exp Zool 194:379–408

    CAS  PubMed  Google Scholar 

  • Tiegs OW (1955) The flight muscles of insects—their anatomy and histology; with some observations on the structure of striated muscle in general. Philos Trans R Soc London Ser B238:221–347

    Google Scholar 

  • Weber T, Moore TE, Huber F, Klein U (1987) Sound production in periodical cicadas (Homoptera: Cicadidae: Magicicada septendecim, M. cassini). Proc 6th Auchen Meeting, Turin, Italy, pp 329–336

  • Wohlers D, Bacon J (1980) Sexual dimorphism of motoneurons: timbal muscle innervation in male periodical cicadas and homologous structures in females. Cell Tissue Res 209:371–382

    CAS  PubMed  Google Scholar 

  • Wohlers D, Williams JLD, Huber F, Moore TE (1979) Central projections of fibres in the auditory and tensor nerves of cicadas (Homoptera: Cicadidae). Cell Tissue Res 203:35–51

    CAS  PubMed  Google Scholar 

  • Young D (1972) Neuromuscular mechanism of sound production in Australian cicadas. J Comp Physiol 79:343–362

    Google Scholar 

  • Young D, Bennet-Clark HC (1995) The role of the tymbal in cicada sound production. J Exp Biol 198:1001–1019

    PubMed  Google Scholar 

  • Young D, Josephson RK (1983a) Mechanisms of sound production and muscle contraction kinetics in cicadas. J Comp Physiol 152:183–195

    Google Scholar 

  • Young D, Josephson RK (1983b) Pure-tone songs in cicadas with special reference to the genus Magicicada. J Comp Physiol 152:197–204

    Google Scholar 

Download references

Acknowledgements

A special thanks to Ms. Cathy Morris for technical assistance with electron microscopy, Dr. Angela Wenning for graphics assistance, and to Dr. Yoland Smith for his generous permission to use the electron microscope facility at the Yerkes Regional Primate Center.

Author information

Authors and Affiliations

  1. Department of Biology, Emory University, Atlanta, GA, 30322, USA

    D. R. Stokes

  2. School of Biological Sciences, University of California at Irvine, Irvine, CA, 92697, USA

    R. K. Josephson

Authors
  1. D. R. Stokes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. K. Josephson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. R. Stokes.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stokes, D.R., Josephson, R.K. Power and control muscles of cicada song: structural and contractile heterogeneity. J Comp Physiol A 190, 279–290 (2004). https://doi.org/10.1007/s00359-003-0490-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-003-0490-3

Keywords

Search

Navigation